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IFT Expert Report on

Emerging Microbiological Food Safety Issues

Implications for Control in the 21st Century

Microbiological food safety is a complex, fundamental issue policy officials, and other interested groups—of the scientific in-
of continuing concern. Contributing to this complexity and formation on emerging foodborne pathogens (from a broad eco-
logical perspective) relative to public policy issues and strategies
the emergence of food safety issues are ongoing changes in for preventing foodborne illness.
demographics, geographic origin of food, food production
This report is the second Expert Report produced by IFT
and processing, food consumption patterns, and microorgan-
since the establishment of its Office of Science, Communica-
isms themselves. These host, environmental, and pathogen tions, and Government Relations, which led the production of
changes challenge our food safety policies and our ability to this report and the IFT Expert Report on Biotechnology and
Foods. In the seven sections of this report, the expert panel fo-
manage food safety throughout the food system.
cuses on the complexity of emerging foodborne pathogens and
factors influencing emergence; manifestation of clinical food-
Recognizing this, the Institute of Food Technologists (IFT), borne disease; human susceptibility; ecology of pathogens in
the 28,000-member nonprofit society for food science and tech- pre-harvest and post-harvest environments; microbial viru-
nology, convened a panel of internationally renowned experts to lence, evolution, selection, adaptation, stress, and driving forces;
review the science related to emerging microbiological food safety risk analysis, the Hazard Analysis and Critical Control Point
issues and implications for their control and to produce a com- system, Food Safety Objectives, microbiological performance
prehensive, scientific report. IFT’s objective for this Expert Report criteria, microbial testing, and surveillance; and steps for man-
is to increase the understanding—among IFT members, senior aging food safety in the future.

Founded in 1939, the Institute of Food Technologists is a nonprofit scientific society with 28,000 members
working in food science, technology, and related professions in the food industry, academia, and government.
As the society for food science and technology, IFT brings sounds science to the public discussion of food issues.
IFT Expert Report Panelists
IFT is deeply grateful to the expert report panelists for the time and effort that each of them expended on this project, bringing
their expertise and insight into the state-of-the-science on the numerous topics addressed in the report. Panelists traveled to Chicago
to participate in full-day meetings and devoted considerable additional time to drafting the report, participating in conference calls to
discuss drafts, and reviewing the drafts. IFT sincerely appreciates these experts’ invaluable dedication to furthering the understanding
of emerging microbiological food safety issues and food safety management.

Morris Potter, D.V.M., Panel Chair Michael Goldblatt, Ph.D. James Lindsay, Ph.D.
Lead Scientist for Epidemiology Director, Defense Advanced Research National Program Leader, Food Safety
Center for Food Safety and Applied Projects Agency Agricultural Research Service
Nutrition Defense Sciences Office, Arlington, VA U.S. Department of Agriculture,
U.S. Food and Drug Administration, Beltsville, MD
Atlanta, GA Craig Hedberg, Ph.D.
Associate Professor, Division of Environ- James Pestka, Ph.D.
Douglas Archer, Ph.D. mental and Occupational Health Professor, Food Science and Human
Professor, Food Science and Human University of Minnesota, Minneapolis Nutrition
Nutrition Michigan State University, East Lansing
University of Florida, Gainesville Dallas Hoover, Ph.D.
Professor, Dept. of Animal and Merle Pierson, Ph.D.
Andrew Benson, Ph.D. Food Sciences Professor, Dept. of Food Science and
Assistant Professor, Food Microbiology University of Delaware, Newark Technology
University of Nebraska, Lincoln Virginia Polytechnic Institute and State
Michael Jahncke, Ph.D. University, Blacksburg
Frank Busta, Ph.D. Associate Professor and Director,
Emeritus Professor, Food Science Dept. of Food Science and Technology Peter Slade, Ph.D.
and Nutrition Virginia Seafood Agricultural Research Director of Research & Technical Services
University of Minnesota, St. Paul and Extension Center at Hampton National Center for Food Safety and
Virginia Polytechnic Institute and State Technology, Summit-Argo, IL
James S. Dickson, Ph.D. University, Hampton
Dept. Chair and Associate Professor, R. Bruce Tompkin, Ph.D.
Dept. of Microbiology Lee-Ann Jaykus, Ph.D. Vice President of Food Safety
Iowa State University, Ames Associate Professor, Food Microbiology ConAgra Refrigerated Prepared Foods,
Dept. of Food Science Downers Grove, IL
Michael Doyle, Ph.D. North Carolina State University, Raleigh
Director, Center for Food Safety Mary Lou Tortorello, Ph.D.
University of Georgia, Griffin Charles Kaspar, Ph.D. Research Microbiologist
Associate Professor, Food Research National Center for Food Safety
Jeffrey Farber, Ph.D. Institute and Environmental Toxicology and Technology
Director, Bureau of Microbial Hazards Center U.S. Food and Drug Administration,
Health Canada University of Wisconsin, Madison Summit-Argo, IL
Ottawa, Ontario, Canada
Arthur P. Liang, M.D., M.P.H.
B. Brett Finlay, Ph.D. Director, Food Safety Initiative Activity
Professor, Biotechnology Laboratory Division of Bacterial and Mycotic Diseases
University of British Columbia, National Center for Infectious Diseases
Vancouver Centers for Disease Control and Preven-
tion, Atlanta, GA

The participants on the expert panel were chosen based on their

scientific expertise. Their contributions represent their individual
scientific perspective and do not represent the perspective of their

IFT Staff
Mary Helen Arthur, M.T.S.C. Rosetta Newsome, Ph.D. Fred Shank, Ph.D.
Lead Editor, Expert Report Director, Dept. of Science and Commu- Vice President, Office of Science, Com-
Dept. of Science and Communications, nications munications, and Government Relations
Chicago, IL Chicago, IL Washington, D.C.


Table of Contents

Introduction ...................................................................................... 4 Development and Dissemination of Resistant Organisms .. 44

Trinity of Factors ..................................................................... 4 Wild-Caught Shellfish and Fish ............................................ 45
Evolution of Controls ............................................................. 4 The Role of Microbiological Indicators in Assuring
Fig. 1a-Foodborne Illness ....................................................... 4 Food Safety ........................................................................ 46
Fig. 1b-Reducing One Factor .................................................. 4 Specific Production Methods ................................................ 47
Fig. 1c-Reducing Multiple Factors .......................................... 4 HARVEST ENVIRONMENT ............................................... 48
Table 1. Evolution of Food Processing .................................... 5 Produce .................................................................................. 48
Evolution of Food Safety Policies ........................................... 5 Food Animals ........................................................................ 48
Microbiology 101 .................................................................... 6 Aquaculture and Wild-Caught Fish and Shellfish ............... 49
Incidence and Prevalence of Foodborne Illness ..................... 8 POST-HARVEST ENVIRONMENT .................................... 49
Emergence of Pathogens ......................................................... 8 Food Animal Slaughter and Meat Processing ...................... 49
Fig. 2. Foodborne Illness Identification .................................. 8 Post-Harvest Processing of Other Commodities ................. 52
Table 2. Foodborne Disease in the United States ................... 9 Water ...................................................................................... 52
Complex Drivers of Change ................................................. 11 Alternative Processing Technologies ..................................... 53
Framework for Food Safety Management ............................ 12 Table 10. Limitations to Alternative Processing
Technologies Currently Under Development ................... 54
Science of Pathogenicity ................................................................ 13 Validation of Treatment Effectiveness Using
Nomenclature ........................................................................ 13
Microbiological Surrogates ............................................... 55
Table 3. Classic Microbial Nomenclature ............................. 13
Transportation and Storage .................................................. 60
Nomenclature of Salmonella and Fig. 3 ................................ 14
Retail and Food Service ......................................................... 61
Virulence ............................................................................... 15
Outbreaks of Shigella sonnei Infection Associated with
Fig. 4. Virulence and Foodborne Illness ............................... 15
Fresh Parsley ...................................................................... 61
Quorum Sensing ................................................................... 16
Microbial Stress Responses to Processing ............................ 62
Virulence of Salmonella ........................................................ 17
Table 11. Conditions That Can Produce Sublethally
Pathogens Are More Than Just Bacteria ............................... 18
Injured Cells ...................................................................... 64
Evolution ............................................................................... 19
New Tools for Pathogen Research ......................................... 64
Fig. 5. Contrasting Views of Pathogen Evolution ................. 20
Ability of Pathogens To Survive in the Environment ........... 66
Fig. 6. Genetic Material in E. coli ........................................... 20
Evolution of Salmonella ........................................................ 21 Application of Science to Food Safety Management ...................... 67
Selection ................................................................................. 21 Risk Assessment .................................................................... 67
Stress ...................................................................................... 22 Risk Management Using Food Safety Objectives ................. 69
F38 Regulated Proteins and Table 4 ....................................... 24 Fig. 7. Framework for Food Safety Management ................. 70
Driving Forces in Pathogenicity ............................................ 25 Hazard Control and Monitoring .......................................... 71
Emergence of Viruses, Parasitic Protozoa and Marine Table 12. FSOs in the Food Safety Management Framework .... 72
Biotoxins as Foodborne Pathogens ................................... 25 Fig. 8. Establishing Performance Criteria ............................. 74
Pathogenicity of E. coli O157:H7 .......................................... 27 Fig. 9. Unequal Levels of Food Safety ................................... 75
Table 13. Probability of Acceptance (Pa) of Defective
Humans as Hosts of Foodborne Disease ........................................ 28
Product Using a 2-class Sampling Plan ............................ 76
Manifestations of Clinical Disease ....................................... 28
Table 14. USDA Monitoring Program for Salmonella ......... 76
Table 5. Causes of Foodborne Illness ................................... 29
Value of Test Results and Fig. 10 ........................................... 77
Pfiesteria piscicida and Pfiesteria-like Microbes as
Testing for Mycotoxins .......................................................... 79
Potential Foodborne Pathogens ........................................ 30
Surveillance for Foodborne Hazards and Illness ................. 79
Resistance to Microbial Foodborne Disease ........................ 31
Outbreak Investigations and New Foodborne Pathogens ... 80
Susceptibility to Microbial Foodborne Disease ................... 34
Animal Surveillance for E. coli O157:H7 .............................. 82
Table 6. Factors That Increase Host Susceptibility ............... 34
Cryptosporidiosis .................................................................. 35 Next Steps in Food Safety Management ......................................... 85
Individual Choices that Affect Disease Risk ......................... 36 Strategic Prioritization to Reduce Foodborne Disease ........ 85
Table 7. Factors That Increase Risk of Foodborne Disease .. 37 Strategies for the Future ........................................................ 87
Modification of Susceptibility ............................................... 39 A Cooperative Approach to the Safety of Sprouts ................ 89
Anticipating the Future: Food Safety Issues on the Horizon ..... 92
Microbial Ecology and Foodborne Disease ..................................... 40
PRE-HARVEST ENVIRONMENT ...................................... 40 Conclusions .................................................................................... 93
Overarching Issues ................................................................ 40
Table 8. Sources of Imported Fresh and Frozen Produce .... 41
References ..................................................................................... 97
Table 9. Percentage of Total U.S. Consumption Provided
By Imports ......................................................................... 41
Typical Pre-Harvest Environment for Foods of Plant Origin ... 42 On the Cover
Production Practices and Mycotoxins .................................. 42 The image on the cover is a scanning electron micrograph of
Typical Pre-Harvest Environment for Foods of Listeria monocytogenes, an emerging foodborne pathogen.
Animal Origin ...................................................................... 43 © 2000 S. Lowry/Univ. Ulster/Stone

The continued occurrence of tific information on emerging foodborne contamination (Fig. 1b). In many cases,
foodborne illness is not evidence of the pathogens relative to public policy issues however, the most effective approach ad-
and strategies for preventing foodborne dresses more than one factor. Current
failure of our food safety system. In illness. technologies and production methods
fact, many of our prevention and cannot provide a food supply that is
control efforts have been—and Trinity of Factors completely free of all pathogenic micro-
organisms. Fortunately, even small re-
continue to be—highly effective. The At the simplest level, foodborne ill- ductions in several factors can have a
U.S. food supply is arguably among the ness can be reduced to three factors: the substantial combined effect (Fig. 1c).
pathogen, the host, and the environment
safest in the world, but significant
in which they exist and interact (see Fig. Evolution of Controls
foodborne illness continues to occur. 1a). Complex relationships exist among
Despite great strides in the area of these factors, and all three factors are New technologies, production prac-
necessary for foodborne illness to occur. tices and food manufacturing processes
microbiological food safety, much For example, a susceptible host may con- are developed to meet the needs of a
remains to be done. sume food that contains a significant changing society. Early food preservation
Foodborne illness is not a simple amount of a microorganism, but if the methods—such as canning, cheese mak-
problem in need of a solution; it is a com- microorganism does not possess the ing, bread making, brewing, fermentation,
plex combination of factors that must be traits necessary to cause illness, food- pickling, salting, and drying—were used
managed on a continual basis. Aside from borne disease does not occur. Similarly, to provide sufficient year-round food
the inherent ability of pathogens them- adequately cooking a food to kill the availability. Later developments reflected a
selves to evolve, pathogens’ victims and pathogenic microbes can eliminate the new focus on food safety, variety, conve-
the microbial environment play a role in exposure factor and render the food safe. nience, and nutritive and sensory quality.
the changing nature of foodborne illness, When one or more of the three fac- At the beginning of the 20th century,
opening new niches and creating new vul- tors changes, new foodborne pathogens contaminated milk, meat, and other
nerabilities. No matter how sophisticated “emerge.” For example, host susceptibil- foods caused large outbreaks and many
and complex a system is developed, food ity can increase so much that existing sporadic cases of foodborne disease, of-
safety management is never finished or microorganisms that do not cause ill- ten with fatal consequences. The revolu-
complete, because change is constant. ness in the general population achieve tion in sanitation and hygiene related to
Recognizing that food safety is a fun- pathogen status in the newly immuno- food and water and the almost universal
damental and continuing issue, the Insti- compromised individuals. The change adoption of thermal pasteurization for
tute of Food Technologists commis- also can be increased virulence, e.g., milk produced tremendous improve-
sioned an expert panel to review the when a microorganism acquires charac- ments in food safety. New technologies
available scientific literature related to teristics that help it invade the human with increasing sophistication have yield-
emerging microbiological food safety is- body. Or it can be new exposure, e.g., ed continued improvements in microbi-
sues. The experts were charged with when fruit from one region carries a ological food safety while delivering bet-
identifying the factors that make a mi- pathogenic microorganism to popula- ter quality foods with greater nutritional
croorganism “emerge” as an important tions in a different geographic region value and superior sensory characteris-
foodborne pathogen and identifying that have never before been exposed. tics (see Table 1).
mechanisms that use this knowledge to This trinity is also the key to reduc- Innovations in packaging have been
improve the safety of our food supply. ing foodborne illness. Prevention and integral to the developments in food pro-
The objective of this report is to increase control efforts often focus on the contri- cessing and product development. Pack-
understanding, among IFT members bution of one of these factors, such as ages contain and protect their food con-
and other interested parties, of the scien- washing vegetables to remove surface tents and inform consumers; they also

Fig. 1a- Foodborne Illness Fig. 1b-Reducing One Factor Fig. 1c-Reducing Multiple Factors


Table 1. Evolution of Food Processing (Goldblith, 1989; IFT, 2000a, 1989; Lund, 1989)

Early times Heating

Cooking food kills many foodborne pathogens
1770s-1800s Canning/Thermal Processing
Significant discoveries in response to industrialization forces and Napoleon’s armies’ need for less dependence on local
1890s Pasteurization
Thermal treatment of raw milk to prevent milk from transmitting pathogens
1920s - 1930s Safe Canning/Processing Parameters
Calculation of product heat penetration curve and initial microbial contamination level to determine minimum time-temperature
combination for commercial sterility
1940s Freezing
Mechanical quick-freezing methods to preserve while maintaining quality
1950s Controlled Atmosphere Packaging
Reduced oxygen levels, increased concentrations of carbon dioxide, or selective mixtures of atmospheric gases to limit
respiration and ethylene production, delay ripening and decay, and increase refrigerated product shelf life
1960s Freeze Drying
Rapid deep-freezing followed by sublimation of water by heating the frozen product in a vacuum chamber. Best known applied
to coffee, to preserve delicate aroma compounds and maintain flavor and odor
1940s-1980s Aseptic Processing and Packaging
High-temperature, short-time sterilization of food product independent of the container, container sterilization, and filling of
product in sterile atmosphere, resulting in increased food quality and nutrient retention
Non-thermal process to kill pathogens, insects, and larvae, inhibit sprouting, and delay ripening and food spoilage
1990s Carcass Spray Treatments (e.g., water, acid), Steam Vacuuming, Steam Pasteurization
Carcass decontamination interventions to meet microbiological performance criteria
High Pressure Processing
Foods subjected to specified pressures and temperatures to preserve food while maintaining quality

preserve, perform, communicate, and sell safety challenges. For example, modified ever-changing challenge both for the in-
(Downes, 1989). From the hermetically atmosphere packaging of fresh packed, dustrialized and the developing world.
sealed containers for shelf-stable foods sliced mushrooms may allow the growth
developed in the early part of the 19th of Clostridium botulinum and potential Evolution of Food Safety Policies
century, to the metal cans for heat-pro- toxin production (Doyle, 1998). Altering
cessed foods, folding cartons, and milk the package, incorporating microscopic Current U.S. food safety policies are
bottles of the latter part of the 19th centu- holes to allow oxygen to permeate the in- the accretions of decades of relatively in-
ry, to the boil-in-bags, plastic tubs, high terior of the packaged product, was an- dependent efforts to address specific
density polyethylene gallon milk jugs, other factor critical to ensuring the safety problems. Most are rooted in the sani-
aseptic cartons, and microwavable poly- of modified atmosphere packaged fresh tary revolution that occurred at the be-
mers of the 20th century, packaging has packed, sliced mushrooms. For extended ginning of the 20th century, and they
played a key role in the development of shelf life refrigerated foods, strict tem- have characteristics that have served us
the food industry in the Western world perature control and acceptable product well during the transition from an agrar-
in the 20th century (Downes, 1989). shelf life are critical factors to consider ian to an industrialized society.
However, changes in technology are (Doyle, 1998). As new technologies are Generally, these regulatory policies
not without risk. Conventional wisdom introduced, they must be evaluated for respond in one of three ways to obvious
of decades ago held that properly refrig- their potential effect on microbiological hazards that pose clear risk to human
erated foods would remain safe because food safety. health. First, for hazards that have
it was thought that pathogenic bacteria Despite all of the significant advanc- straightforward technical fixes, regula-
would not grow at refrigeration tempera- es to date, our growing knowledge base tions require the application of the ap-
tures, but this is not always the case continues to expose the role of various propriate technologies. Regulatory stan-
(Marth, 1998). Innovations in food pro- foods and technological innovations in dards frequently have been set at the per-
cessing, such as modified atmosphere foodborne hazards, and changes in the formance limit of the technology or the
packaging, can offer the benefit of greatly food, the consuming public, and the detection limit for the analytical test used
extending the shelf life of refrigerated pathogens themselves continue to make for process verification. However, tech-
foods but may present microbiological foodborne disease an important and nologies to mitigate hazards are not al-

ways apparent. In these cases, the regula- C. botulinum. Another very successful major challenges to food safety policy
tory response has been to either keep the example is the water quality standards formulation. Factors like the global
hazardous food out of the marketplace for shellfish growing waters. These sourcing of products and ingredients,
or to forgo regulatory action and rely on standards protected consumers from changes in land use, and evolution of
prudent people to protect themselves. shellfish-associated typhoid fever at a science and technology have radically
Numerous food safety concerns time when typhoid was fairly common changed hazards associated with a par-
have been successfully addressed by this in coastal communities and contami- ticular food and the control options
regulatory paradigm. The promulgation nated shellfish was an important source available.
of regulations for low acid canned food of infection. Historically, the safety of These challenges present themselves
virtually ended the historic association foods without a pathogen elimination in many ways depending on the particu-
of botulism with commercially canned step earlier in the line has depended lar hazard. For example, the indicator or-
food. Under the regulations, commer- upon proper cooking. ganisms used to predict the presence of
cially canned foods undergo a mini- The extraordinary complexity of Salmonella Typhi in shellfish growing
mum calculated destruction of 12D for contemporary food safety issues presents waters poorly predict the presence of

Microbiology 101 most successful life form. Their diversity teriorates, the spore is released into the
and “complexity through simplicity” environment. Spores are extremely im-
The characteristics of the various have and will continue to assure their pervious to physical and chemical harm,
microorganisms are part of what survival. Although the vast majority of making them difficult to inactivate in the
makes microbiological food safety is- bacteria are harmless or helpful to hu- food processing environment.
sues so complex. One type of micro- mans, some are pathogenic. In general, the bacterial kingdom can
organism may thrive under condi- be divided into gram-positive and gram-
tions that are fatal to a different mi- Eukaryotes—Parasites and Fungi negative cells. These designations are
crobe. Some microbial pathogens given based on the results of a staining
cause disease by infecting the human Eukaryotes are multicellular living procedure that separates the two divi-
host, while others produce toxins that organisms that possess a nuclear mem- sions by color, which is reflective of the
cause illness. Some pathogens can brane that separates their nucleic acid composition of their cell wall.
multiply in food during storage while from the cytoplasm. They are larger than
others cannot. Because most micro- bacteria and are sometimes able to be Growth and Life Span
organisms can reproduce within a seen by the human eye. Eukaryotes are Bacteria—Bacteria are the most
matter of minutes, these pathogens generally free-living in the environment. adaptable life form on Earth. Bacteria
can evolve quickly when environ- Some protozoa can be foodborne have “optimal” (preferred) growth condi-
mental stresses select for strains with pathogens (e.g., Cyclospora, Giardia). tions, but some can grow and/or survive
unique survival characteristics. They usually exist in multiple forms, at extremes of temperature, pH, osmotic
some of which are environmentally sta- pressure, and barometric pressure. Bacte-
Types of Microorganisms ble, but they seldom multiply in or on ria are genetically programmed for maxi-
human food. Fungi such as molds and mum survival.
Microorganisms are divided into yeasts can multiply in or on human food At optimal growth conditions, a bac-
three distinct categories: prokaryotes, and also can be pathogenic. terial cell may divide every 10-20 min-
eukaryotes, and viruses. Both utes. Assuming no death, a single cell
prokaryotes and eukaryotes are highly Viruses could thus give rise to a bacterial mass
regulated cells that possess elaborate equal to the Earth’s mass in one or two
“sensing” systems, enabling them to be Foodborne pathogenic viruses are days. Obviously death occurs, because of
aware of and react to their environ- comprised of a single type of nucleic factors such as nutrient limitations or
ment as it changes. acid surrounded by a protein coat. Vi- end product toxicity.
ruses are not free-living. In fact, they Viruses—In general, viruses
are not living beings at all, but are obli- reproduce more rapidly than bacteria,
Prokaryotes—Bacteria gate intracellular parasites. They are but they can only grow in an infected
Prokaryotes are single-celled living smaller than bacteria (10-350nm), and host cell, not in food. A single infected
microorganisms that have no nuclear some viruses prey on bacteria (bacte- host cell may give rise to hundreds or
membrane separating their genetic riophages). thousands of new viruses within a few
material from the cytoplasm within hours, each of which may infect a new
the cell. They are microscopic, in that Types of Bacteria host cell.
they cannot be seen with the unassist-
ed human eye. Bacteria are generally Bacteria come in various shapes, Roles of Foodborne
free-living in the environment, al- such as rods, spheres (cocci), and spirals. Microorganisms
though some have complex nutrient As a response to certain adverse environ-
requirements and can grow only in mental conditions, some bacteria can Not all microorganisms in foods are
special niches. form spores. The spores start as dense harmful. In fact, only a small proportion
Bacteria are arguably the world’s regions within the cell, but as the cell de- of foodborne organisms have been asso-


Vibrio, hepatitis A, or Norwalk-like vi- cooking will kill this parasite, the foods Modifications to thermal processing
ruses. Typhoid fever is now extremely associated with human infection—rasp- have made a wide array of food types
uncommon in U.S. coastal waters, and it berries, basil, and other fresh produce— possible, including a proliferation of
is now these other shellfish-associated are generally not cooked before con- “pasteurized” food products distributed
pathogens from which we need to protect sumption. in flexible plastic packages that require
ourselves. When microorganisms such as Shigel- refrigeration. Although thermal process-
Pathogens on foods that are often la or the hepatitis A virus are found on ing inactivates a large majority of the
consumed without cooking present a fresh produce, it can be difficult to deter- vegetative spoilage organisms, in con-
significant challenge. The pathogen Cy- mine whether the contamination oc- trolled atmosphere packaging, it also
clospora cayetanensis is very likely of curred during food preparation, during drives off oxygen and fails to inactivate
human origin, but our limited knowl- distribution, during processing and pack- sporeformers like C. botulinum. If the
edge about its natural ecology does not ing, or in the growing fields. Under these cold chain is not properly maintained,
enable us to assure its absence from circumstances, the appropriate point of botulinum toxin can be produced before
fresh produce. Although adequate intervention is difficult to identify. food spoilage is detectable.

ciated with disease in normal, healthy cause spoilage. For instance, spoilage of organisms that are associated with dis-
animals and humans. raw meats is almost always associated ease in humans and/or animals. Patho-
with gram-negative psychrotrophs, the genic microbes are capable of causing ill-
Commensal Microbes so-called cold-thriving organisms, be- ness, either by infecting the host or by
cause they grow at refrigeration temper- producing toxins that cause the host to
Virtually all raw food contains mi- atures. Fresh fruits are frequently become ill. Some microorganisms are
croorganisms. The source of these is the spoiled by yeasts and molds that are pathogenic in one host species but not in
production environment, where a wide able to thrive in acidic conditions. Most another. For example, Escherichia coli
variety of organisms are environmentally spoiled foods do not cause foodborne O157:H7 causes illness in humans but
ubiquitous. Processing and handling of disease; in reality, the high levels of not in cattle, its primary host.
foods can also contribute to the types spoilage organisms have frequently
and numbers of commensal organisms “out-competed” the pathogens, keeping Microbiological Indicators
on foods. Most of these commensal or- pathogen growth in check.
ganisms are harmless to animals and hu- An index or indicator refers to a
mans; in fact, they may actually be bene- Beneficial Microbes single or group of microorganisms, or
ficial in that they provide high levels of alternatively, a metabolic product,
“competitive” microflora that usually Perhaps the most widely recognized whose presence in a food or the envi-
grow faster than contaminating patho- group of beneficial foodborne microor- ronment at a given level is indicative
gens. Although the purpose of many ganisms are the members of the lactic acid of a potential quality or safety prob-
bacteria (LAB) group. This is a functional lem. Microbiological indicators are
common food processing methods such
name used to classify fermentative organ- used in place of direct testing for a
as pasteurization and canning is the de-
isms that produce lactic acid as the prima- pathogen, largely because they are
struction of pathogens, commensal mi-
ry by-product of metabolic activity, al- easier to work with. Indicators may
croorganisms are often destroyed in the
though other products, such as alcohol be a specific microorganism (e.g., E.
process as well.
and carbon dioxide may be produced as coli), a metabolite (e.g., lactic acid ti-
well. These metabolic products are re- tration), or some other indirect mea-
Spoilage Microbes sponsible for the characteristic flavor, sure (e.g., ATP bioluminescence as a
odor and texture of fermented food prod- measure of sanitation efficacy). Using
Spoilage may be defined as a condi- ucts. The lactic acid bacteria are com- a specific microorganism as an indi-
tion in which food becomes inedible be- monly used in dairy, vegetable and meat cator is difficult, because appropriate
cause of undesirable changes in color, fermentations. Notable members of this indicator organisms are difficult to
flavor, odor, appearance, and texture. group belong to the Lactococcus, Lactoba- identify. An “ideal” indicator organ-
This condition occurs primarily be- cillus, Pediococcus, and Leuconostoc genera. ism: (1) has a history of presence in
cause the organisms grow to high levels, Some species of yeasts and molds can also foods at any time that the target
producing enzymes that break down be used in the commercial production of pathogen or toxin might be present;
food components such as fats, proteins, fermented foods, including Saccharomyces (2) is present at concentrations di-
and sugars. In most instances, spoilage cerevisiae, used frequently for producing rectly related to that of the target
is caused by commensal organisms that bread, beer and wines, and Aspergillus pathogen or toxin; (3) is absent from
have been allowed to reach populations oryzae, used in the fermentation of orien- food when the target is not present;
in the range of 105 to 107 CFU/g of tal foods such as soy sauce. (4) has growth rates equivalent to, or
food. Different classifications of foods slightly greater than, the pathogen;
(such as red meats, vegetables, fish, etc.) Foodborne Pathogens (5) has rapid, simple, and inexpensive
have different spoilage profiles because quantitative assays available; (6) has
the food environment will dictate which Foodborne pathogens encompass a similar resistance profiles to the tar-
organisms will grow, dominate, and relatively small group of foodborne micro- get; and (7) is nonpathogenic.

Non-thermal processes also have than half of all recognized foodborne dis- nally, some proportion of foodborne ill-
been modified over time. Consumers ease outbreaks have unknown causes, in- ness is caused by pathogens that have not
want foods with fewer preservatives, less dicating the real number of disease-caus- yet been identified and thus cannot be
salt, fewer calories, and better texture; the ing agents is likely much larger than 200. diagnosed. In fact, many of the patho-
food industry has responded with many The recognized causes of foodborne ill- gens of concern today were not recog-
new formulations. However, substitut- ness include viruses, bacteria, parasites, nized as causes of foodborne illness just
ing ingredients with gums or other fat re- manmade chemicals, biotoxins, heavy 20 years ago (Mead et al., 1999).
placers and reducing salt or sugar can re- metals, and prions. The symptoms of New scientific advances make it pos-
quire a reevaluation of food safety con- foodborne illnesses range from mild gas- sible to approach foodborne illness from
trol measures. For example, the replace- troenteritis to life threatening neurologic, a different, broader perspective. More
ment of sugar with an alternative sweet- hepatic, and renal syndromes. powerful diagnostic procedures and bet-
ener in hazelnut yogurt and failure to In the United States, foodborne dis- ter communication technology allow im-
evaluate the impact of this change on eases have been estimated to cause ap- proved tracking and surveillance for
food safety resulted in an outbreak of proximately 76 million illnesses, foodborne illness. Genetic identification
botulism (O’Mahony et al., 1990). 325,000 hospitalizations, and 5,000 methods allow scientists to link geo-
In addition to the impact of changes deaths each year (Mead et al., 1999). A graphically distinct outbreaks of food-
in processing, scientists have discovered pathogen’s ability to cause illness can be borne illness to a single source. Patho-
that some foodborne pathogens survive very different from the severity of the gens can appear to emerge simply be-
traditional processes better than expect- illness it causes. Some pathogens such cause scientists develop methods to iden-
ed. For example, Salmonella have been as Norwalk-like viruses cause a great tify the presence of certain microorgan-
found in 60-day aged cheese and on raw number of illnesses (9.2 million per isms and link them to foodborne disease.
almonds, and newly recognized patho- year) but the fatality rate is very small New technologies based on recent
gens such as E. coli O157:H7 are more (0.001%) (see Table 2). Others such as advances in genomics also give scientists
tolerant of conditions of low pH and Vibrio vulnificus cause few illnesses (47 greater insight into pathogen virulence
other traditional barriers than antici- per year), but many of those illnesses and evolution, opening the door to better
pated. The resistance of pathogens to are fatal (38.3%). Salmonella, Listeria controls and therapeutics. Future scien-
traditional treatments affects the safety monocytogenes, and Toxoplasma gondii tific advances will continue to enhance
of our drinking and processing water as are responsible for more that 78% of efforts to identify and understand food-
well. We have relied on chlorination to the deaths but only approximately 11% borne pathogens, and these insights will
rid drinking water of pathogens for de- of total cases of foodborne disease. The contribute the data necessary for science-
cades, but recent waterborne outbreaks issue is further complicated by patho- based risk assessment and food safety
have been caused by parasites, such as gens, such as L. monocytogenes, that management.
Giardia and Cryptosporidium, that are cause little or no illness in healthy indi-
not controlled by chlorine. viduals but cause severe illness and Emergence of Pathogens
Handling during preparation in the death in sensitive populations, includ-
home or foodservice establishment may ing the immunosuppressed, the elderly The terminology “newly emerging
affect the pathogens present in the food. and the developing fetus. Prioritizing pathogen” has become somewhat over-
For foods in which preparation should food safety resources can be difficult. used, or perhaps it is merely ill defined.
kill the pathogens, recurring outbreaks of Scientists gather data about the inci- True pathogen “emergence” could be di-
foodborne illness highlight our limited dence and severity of foodborne illness rectly linked to evolution, whether that
ability to tightly control food preparation through surveillance, both passive and evolution occurs gradually or rapidly.
behaviors and practices. Certainly the in- active. Mild cases of illness often are not In a broader context, emergence can
cidence of foodborne disease would be captured by surveil-
significantly reduced if we could eliminate lance programs because Fig. 2. Foodborne Illness Identification
pathogens earlier in the food chain. How- medical intervention is
ever, the initial number of the pathogen in not required for recov- Sick individual seeks medical attention.
the food is only one factor in the risk of ery. Many steps are re-
foodborne illness. At some point, im- quired for a foodborne
provements in sanitation will produce pathogen to be identi- Clinician considers cause to be foodborne,
only small incremental gains. As the level fied as the cause of ill- requests proper tests and collects appropriate specimen.
of contamination becomes increasingly ness and for data to be
small, other food safety approaches will gathered through sur- Proper test is performed correctly.
need to be adopted. veillance programs (see
Fig. 2). Furthermore, Results are reported to the health department
Incidence and Prevalence of because many patho- and ultimately the CDC.
Foodborne Illness gens transmitted
through food also may
Food safety is a complex issue that de- be spread by contami- Regulatory agency investigates.
pends on a number of interrelated envi- nated water and per-
ronmental, cultural, and socioeconomic son-to-person contact, Identification of the source of the illness
factors. More than 200 known diseases the role of food can be prompts product recall or other action.
are transmitted through food, and more difficult to assess. Fi-



Table 2. Foodborne Disease in the United States, Including Estimated Annual Prevalence (FDA/CFSAN, 2002; Mead et al., 1999)
Microorganism Principal Symptomsa Onseta Potential Food Contaminationa Illnessesb Deathsb
Bacillus cereus 27,360 0
Diarrheal—Watery diarrhea, abdominal cramps and pain 6-15 hr Meats, milk, vegetables and fish n/a n/a
Emetic—Nausea and vomiting 0.5-6 hr Rice products, starchy foods (e.g., potato, pasta, and cheese products n/a n/a
Brucella spp. Sweating, headache, lack of appetite, fatigue, feverc Days to weeksc Raw or unheated processed foods of animal origin (e.g., milk, milk 777 6
products, cream, cheese, butter)c
Campylobacter spp. 1,963,141 99
C. jejuni Watery diarrhea, fever, abdominal pain, nausea, headache, 2-5 days Raw chicken, beef, pork, shellfish; raw milk n/a n/a
muscle pain
Clostridium botulinum Weariness, weakness, vertigo, double vision, difficulty 18-36 hr Improperly canned or fermented goods 58 4
swallowing and speaking
Clostridium perfringens Intense abdominal cramps, diarrhea 8-22 hr Meat, meat products, gravies 248,520 7
Escherichia coli
Enterotoxigenic Watery diarrhea, abdominal cramps, fever, nausea, malaise 24 hr Foods contaminated by human sewage or infected food handlers 55,594 0
Enteropathogenic Watery or bloody diarrhea n/a Raw beef and chicken; food contaminated by feces or contami- n/a n/a
nated water
E. coli O157:H7 Severe abdominal cramps, watery or bloody diarrhea, 1-2 days Undercooked or raw hamburger, alfalfa sprouts, unpasteurized juices, 62,458 52
hemolytic uremic syndrome dry-cured salami, lettuce, game meat, cheese curds, raw milk
Enteroinvasive Abdominal cramps, vomiting, fever, chills, generalized 12-72 hr Food contaminated by human feces or contaminated water, n/a n/a
malaise, hemolytic uremic syndrome hamburger meat, unpasteurized milk
Listeria monocytogenes Nausea, vomiting, diarrhea; influenza-like symptoms; Few days- Raw milk, cheeses (particularly soft-ripened varieties), raw 2,493 499
meningitis, encephalitis; septicemia in pregnant women, 3 weeks vegetables, raw meats, raw and smoked fish, fermented sausages
their fetuses or newborns; intrauterine or cervical infection
that may result in spontaneous abortion or stillbirth
Salmonella spp. Raw meats, poultry, eggs, milk and dairy products, fish, shrimp, n/a n/a
frog legs, yeast, coconut, sauces and salad dressings
S. Typhi and S. Paratyphi Typhoid-like fever, malaise, headache, abdominal pain, body 7-28 daysc 659 3
aches, diarrhea or constipation
Other Salmonella spp. Nausea, vomiting, abdominal cramps, fever, headache; 6-48 hr 1,341,873 553
chronic symptoms (e.g., arthritis) 3-4 weeks
Shigella spp. Abdominal pain and cramps; diarrhea; fever; vomiting; 12-50 hr Salads (potato, tuna, chicken, macaroni), raw vegetables, bakery 89,648 14
blood, pus or mucus in stools; tenesmus products (e.g., cream-filled pastries), sandwich fillings, milk and
dairy products, poultry
Staphylococcus aureus Nausea, vomiting, retching, abdominal cramps, prostration 1-7 hr Meat and meat products, poultry, egg products, salads (egg, tuna, 185,060 2
chicken, potato, macaroni), cream-filled bakery products, milk and
dairy products
Streptococcus spp. 50,920 0
Group A (S. pyogenes) Sore, red throat; pain on swallowing; tonsillitis; high fever; 1-3 days Temperature-abused milk, ice cream, eggs, steamed lobster, ground n/a n/a
headache; nausea; vomiting; malaise; rhinorrhea ham, potato salad, egg salad, custard, rice pudding, shrimp salad

a n/a indicates FDA/CFSAN (2002) did not provide information.

b n/a indicates Mead et al. (1999) did not provide an estimate for this pathogen.
c As described by ICMSF (1996).

Table 2. Foodborne Disease in the United States, Including Estimated Annual Prevalence, continued

Microorganism Principal Symptomsa Onseta Potential Food Contaminationa Illnessesb Deathsb

Group D (other Streptococcus Diarrhea, abdominal cramps, nausea, vomiting, fever, chills, dizziness 2-36 hr Underprocessed or improperly prepared sausage, evaporated n/a n/a
spp.) milk, cheese, meat croquettes, meat pie, pudding, raw milk,
pasteurized milk
Vibrio cholerae 49 0
V. cholerae serogroup O1 Mild watery diarrhea, acute diarrhea, rice-water stools 6hr-5 days Raw, improperly cooked, or recontaminated shellfish n/a n/a
V. cholerae serogroup non-O1 Diarrhea, abdominal cramps, fever, vomiting, nausea; blood or mucus- 48 hr Raw, improperly cooked, or recontaminated shellfish n/a n/a
containing stools
Vibrio parahaemolyticus Diarrhea, abdominal cramps, nausea, vomiting, headache, fever, chills 4-96 hr Raw, improperly cooked, or recontaminated shellfish and fish n/a n/a
Vibrio vulnificus Fever, chills, nausea, septicemia in individuals with some underlying 16 hr Raw or recontaminated oysters, clams, crabs 47 18
diseases or taking immunosuppressive drugs or steroids
Vibrio, other n/a n/a n/a 5,122 13
Yersinia enterocolitica Fever, abdominal pain, diarrhea and/or vomiting 24-48 hr Meats, oysters, fish, raw milk 86,731 2
Parasites and Protozoa
Anisakis simplex Tingling or tickling in the throat, vomiting or coughing up worm(s), 1hr-2 weeks Raw or undercooked seafood n/a n/a
abdominal pain, nausea
Ascaris lumbricoides Exiting of roundworm, vague digestive tract discomfort, pneumonitis n/a Raw produce grown in soil contaminated by insufficiently n/a n/a
treated sewage
Cryptosporidium parvum Severe watery diarrhea (intestinal illness); coughing, fever and intestinal 1-12 days Foods contaminated via food handlers and manure 30,000 7
distress (pulmonary and tracheal illness)
Cyclospora cayetanensis Watery diarrhea, explosive stools, loss of appetite, bloating, stomach 1 week Water or food contaminated with infected stool 14,638 0
cramps, vomiting, aching muscles
Giardia lamblia Diarrhea, abdominal cramps, bloating, weight loss, malabsorption 1 week Food contaminated via infected food handlers 200,000 1
Taenia spp. Discharge of proglottids, anal itching, abdominal pain, nausea, weakness, n/a Raw or undercooked beef, pork n/a n/a
weight loss, intestinal disorder
Toxoplasma gondii Flu-like symptoms, swollen lymph glands, muscle aches and painsd 10-23 daysd Raw or undercooked meats, especially pork, lamb, 112,500 375
Trichinella spiralis Severe gastrointestinal distress, nausea, vomiting, headaches, weakness, 3-14 days venisond 52 0
muscle pain, chills, difficulty breathing, body swelling, visual deficiencies, Raw or undercooked pork or wild game
fever, night sweatingc

Hepatitis A Fever, anorexia, malaise, nausea, abdominal discomfort; jaundice may 10-50 days 4,170 4
follow Shellfish, salads, other foods contaminated via infected
Norwalk-like viruses Nausea, vomiting, low-grade fever, diarrhea, abdominal pain 24-48 hr food handlers or water 9,200,000 124
Shellfish and salad ingredients contaminated by infected
Rotavirus Vomiting, watery diarrhea, low-grade fever; severe in infants and young 1-3 days food handlers or fecally contaminated water 39,000 0
children Foods contaminated via fecal contaminated food handlers

a n/a indicates FDA/CFSAN (2002) did not provide information.

b n/a indicates Mead et al. (1999) did not provide an estimate for this pathogen.
c As described by ICMSF (1996).
d From CDC (2002).
be used to describe a recent significant been essentially eliminated; however, cas- Stresses can create microorganisms with
change. Using this interpretation, a es of botulism in the late 1980s and early greatly enhanced mutation frequencies
pathogen could be described as emerging 1990s led scientists to discover that C. (1000-fold or more). The large number
when it is first linked to disease, when the botulinum could grow and produce tox- of different mutations increases the
illness it causes suddenly increases in ins in foods such as twice-baked pota- chance of a mutation that will enable
frequency or severity, or even when a toes, grilled onions, and garlic-in-oil. survival in the stressful environment.
pathogen recognized for a significant When these new food associations were These hypermutable microorganisms
amount of time suddenly “reappears.” In discovered, even C. botulinum was de- also may more readily share DNA with
terms of public perception, all these sce- scribed by some as an emerging patho- other microorganisms, even remotely re-
narios may be considered emerging mi- gen. Large outbreaks—although recur- lated species. Horizontal transmission
crobiological food safety issues. rences of situations that have happened of genetic material from one microor-
in the past—can propel a pathogen to ganism to another can result in quantum
Public Perception of Emergence “emerging” status whether truly deserved jumps in evolution. Gene transfer be-
or not. In many cases, it is the new food tween separate lineages of a bacterial
C. cayetanensis, a recent arrival in vehicle that is the surprise, and not so pathogen can lead to the emergence of
the United States, is an example of the much the pathogen itself. altogether new pathogens. Recently se-
kinds of surprises that can occur as a quenced bacterial genomes reveal more
result of increasing world trade in Emergence as a Function of Evolution extensive exchange of genetic material
ready-to-eat foodstuffs. As foodstuffs between species than had been expected.
are transported ever greater distances, Evolution can produce pathogens
pathogens can be transported to new that are truly emerging, in that the mi- Complex Drivers of Change
areas as well. The United States also has croorganisms have new characteristics
experienced illness outbreaks caused by that enable them to cause disease. Bacte- No matter how emergence is defined,
Salmonella serotypes either rarely or ria have evolved highly sophisticated sig- it becomes clear that the interrelation-
never before isolated here, apparently nal transduction systems that allow the ship of pathogen, host and environment
for the same reason(s) that Cyclospora microorganisms to respond at a genetic plays a key role in microbiological food
“emerged.” level to environmental conditions in a safety. A number of factors will drive the
Campylobacter jejuni and L. monocy- coordinated manner. The many envi- emergence of new food safety concerns,
togenes were well accepted as foodborne ronmental stimuli that trigger such activ- including changes in the characteristics
pathogens in the 1970s and 1980s, re- ity are collectively referred to as stresses. of the consuming public, changes in the
spectively, and, as such, they are hardly The genetic response to stress(es) can foods we manufacture and sell, changes
new. Prior to 1972, C. jejuni could not be activate certain virulence determinants, a in the hazards themselves, and changes
cultured from feces, so it was not recog- microbe’s “contingency plan” for surviv- in the ability of public health officials to
nized as a common human pathogen, nor ing in hostile environments. Beyond ac- identify illnesses as foodborne and to
was the frequency of its presence in food, tivating virulence determinants, external trace the illnesses to their food source.
particularly raw poultry, realized. With stresses also accelerate the bacteria’s rate
improvements in both the sensitivity and of evolution, meaning new pathogens Host Factors
rapidity of the available methodology, C. could “emerge” relatively quickly. Such
jejuni may appear to be an emerging events probably contributed substantial- Changing demographic characteris-
pathogen. However, scientists cannot de- ly to the evolution of the highly virulent tics of consumers affect the number of
termine if the frequency of C. jejuni isola- O157:H7 strain of E. coli. cases of foodborne illness. As the
tion from human stool or food is truly in- Bacteria are constantly mutating, and world’s population continues to grow,
creasing, or if laboratory-induced bias environmental forces may select a muta- constant rates of disease will increase the
gives the appearance of an increase. Simi- tion that confers an advantage in the face total number of cases. In addition, the
larly, methods for isolation of L. monocy- of the environmental challenge. The proportion of the population that is at
togenes from foods and the environment many and varied environmental stresses high risk of foodborne infections, illness,
have improved since its “emergence” as a commonly include starvation, high or and death is rising. Factors that increase
foodborne pathogen in the mid-1980s. As low pH, oxidation, heat, cold, and os- the impact of foodborne diseases include
a result, it appears that the frequency of L. motic imbalance. The genetic response age, chronic diseases, immunosuppres-
monocytogenes in foods and the environ- to one stress may protect the microbe sive conditions, and pregnancy. The im-
ment is increasing, but the influence of from a different stress, a phenomenon mune system functions less effectively in
laboratory-induced bias is difficult to known as cross protection. the elderly, putting them at greater risk. A
weigh. For both of these pathogens, in- Bacteria possess specific genetic loci, growing proportion of our population is
creased awareness of analytical laboratory particularly in “contingency genes,” that immunocompromised due to HIV infec-
personnel and physicians have affected the are highly mutable when compared with tion, cancer chemotherapy, and drugs
frequency of isolation from foods and di- “housekeeping genes” that are relatively used to combat rejection of transplanted
agnosis of human illness. stable. Contingency genes help a mi- organs. Larger numbers of people with
Changes in foods serving as vectors crobe successfully interface with envi- chronic diseases, like diabetes, now live
have brought new attention to a long- ronmental change, while housekeeping longer and also are at increased risk of
recognized pathogen, C. botulinum, the genes run the routine cellular machinery. foodborne diseases.
causative agent of botulism. Botulism Genetic variation can occur in many Other consumers are at elevated risk
from commercially canned foods has ways, including increased mutation. of foodborne illness because of the in-

creased likelihood of exposure. This ele- imported into the United States and beginning to clarify the very basis of the
vated risk is sometimes due to food pref- Canada from Guatemala. interaction between humans and the mi-
erences based on ethnicity, age, or gender. croorganisms that can make us sick.
Young adult males, for example, are Pathogen Factors Industrialized and developing nations
more likely to eat inadequately cooked have improved their ability to conduct
ground beef. Stable and accurate transfer of genet- surveillance and investigate outbreaks of
ic information from parent to offspring disease in humans during the last two de-
Environmental Factors is essential for the preservation of a spe- cades of the 20th century, and this progress
cies. However, keeping pace with an is continuing. In addition, the combina-
Food industry economics and tech- ever-changing environment also requires tion of molecular biology and electronic
nical factors continue to drive consolida- variability. When naturally occurring information technology in centers around
tion in primary agricultural production bacteria, for example, divide, most of the the globe is refining the quality of the data
and food processing. Although this offspring look and act just like their par- that links cases together around common
helps reduce costs and assure uniform ents, but a small proportion of the off- exposures. National and multinational
quality, when a large lot of a contaminat- spring mutate, increasing the chance that networks of collaborators are being
ed food enters distribution, the scope of some might survive in a new, hostile en- pulled together with help and guidance
the resulting outbreak is increased. vironment. If the environment has not from the World Health Organization and
Global sourcing also carries the po- changed, these new strains may not sur- the Food and Agriculture Organization
tential to move pathogens and toxins vive, but this natural occurrence makes it of the United Nations, to facilitate the
from areas in which the pathogen is in- almost certain that traditional food pro- rapid sharing of data.
digenous to areas in which it has not pre- cesses will fail to deliver their predicted The process of ensuring the safety of
viously existed. Unfamiliarity compli- level of safety at some point. This is part food is dynamic as well as complex.
cates diagnosis and containment and can of nature and happens without human Changes in the types of food that are con-
result in outbreaks that become quite intervention. sumed, the geographic origins of food
large before they are recognized. Haz- In addition to this unstimulated hy- products, and the ways in which different
ards are truly mobile, and our food safe- permutability, the food production and foods are processed affect both the risk for
ty programs must be very agile to reduce processing environment can increase the contamination and the adequacy of safety
our risk. rate of change in foodborne pathogens. measures. The processes used to control
Even slight increases in environmen- Bacterial stress responses may increase foodborne hazards to limit the potential
tal temperatures can significantly affect pathogen virulence, and other actions for foodborne disease must be continu-
the risk of foodborne illness. The growth can affect which microorganisms survive ously reviewed and judged against new
of algae in surface waters, estuaries, and and dominate in a particular environ- information and new hazards. Advances
coastal waters is sensitive to temperature. ment. For example, use of antimicrobial in risk assessment methodologies and
About 40 of the approximately 5,000 agents during livestock production may availability of additional data make it pos-
known species of marine phytoplankton select resistant strains from a back- sible to integrate information from the
(algae) can produce biotoxins, which ground of susceptible microorganisms, various stages in the food production
may reach human consumers through increasing the likelihood that the micro- process for those foodborne hazards we
shellfish. Warmer sea temperatures can organisms in a food are resistant to those know about. This capability can be used
encourage a shift in species composition and related antimicrobials. Even if these to identify particular steps in the food
of algae toward the more toxic di- microorganisms are not pathogenic, they supply system for targeted intervention to
noflagellates. Upsurges of toxic phy- can share the genetic material that en- control hazards and prevent disease. It is
toplankton blooms in Asia are strongly ables them to resist antimicrobials with more difficult to provide specific advice
correlated with El Niño, and in the Unit- pathogenic microorganisms in the hu- on how to prevent foodborne hazards that
ed States, paralytic shellfish poisoning man gut, producing pathogens that cause have not yet been identified.
and other marine biotoxin-induced dis- infections that may be difficult to treat.
eases have been associated with shell Through improved laboratory tech- Framework for Food Safety
stock harvested from beds traditionally niques, scientists are identifying adverse Management
considered safe. health effects associated with ever-small-
Consumer desires drive food prod- er levels of exposure to natural and an- Our existing approach to food safety
uct development. Food manufacturers thropogenic substances. New ELISA and management has given the United States
respond to desires for “fresher” food, radioimmunoassays for various myc- an extremely safe food supply. However,
low fat products, or ready-to-eat foods otoxins are pushing tolerances for com- estimates of the incidence of foodborne
by developing new processes or refor- mon mycotoxins down and are finding illness clearly show that, in some cases,
mulating existing products. Changes in more poorly characterized mycotoxins the existing approach to control is inade-
the food processing environment or in a broad array of commodities. Our quate. The complex, ever-changing na-
product formulations can create a new understanding of biology, however, is ture of microbiological food safety guar-
niche for pathogenic microorganisms. not keeping up with our laboratory antees that new challenges will continue
Producing familiar foods in nontradi- skills, and judging the public health sig- to emerge.
tional sites also may lead to introduc- nificance of “positive” laboratory results Microbiological food safety is not an
tion of new food hazards; such was the is becoming more difficult. Unlocking issue only for microbiologists. Just as the
case with the first outbreaks of cy- the human genome and the genomes of farm-to-table approach to food safety
closporiasis associated with raspberries pathogenic microorganisms, however, is has provided an overall picture of food


safety management, many scientific dis- too must our management strategies and management framework should use food
ciplines contribute to our knowledge our regulatory framework. Regulatory safety objectives to translate data about
about food safety. The scientific commu- programs must be flexible to address is- risk into achievable public policy goals.
nity must pull together multidisciplinary sues as they arise and to benefit from sci- Microbiological food safety issues
teams that combine microbiology, epide- entific advances. Continued research will will continue to emerge. Although we
miology, genetics, evolutionary biology, improve our understanding of the com- cannot expect to accurately predict the
immunology and other areas of expertise plex factors that cause foodborne illness, details of complex changes such as
to enhance our understanding of the in- and surveillance programs will gather pathogen evolution, scientific knowledge
terrelated factors that drive emerging data to document the effectiveness of our can be used to identify the areas of great-
food safety issues. controls and identify new problems as est concern, so that we may be ready to
Just as the issues change over time, so they emerge. A science-based food safety respond as issues arise.

Science of Pathogenicity
Pathogenicity is the ability to cause entists understand how a particular ity poorly or that cluster pathogenic and
illness. Because pathogens are living pathogen is able to cause illness, then nonpathogenic microbes together under
they can look for ways to disrupt this one name.
organisms that rapidly adapt and
process and render the microorganism The names used to describe various
evolve, the methods they use to cause harmless or find treatments that mitigate microbiological foodborne pathogens
illness are never static. Pathogen illness. The very factors that create are based on systematic nomenclature. It
evolution is continuous and is driven pathogenicity are opportunities for con- is common practice to identify an organ-
trol. Just as the pathogens adapt and ism based on its genus and species. To
by a variety of forces, only some of evolve, so can our understanding and provide additional detail, classifications
which relate to human activities. The our response. such as subspecies, strain, serotype,
continual evolution of foodborne pathovar, and toxin type may be used
pathogens forces us to change food
Nomenclature (see Table 3).
In the past, the classification of mi-
production processes and products to Traditionally, the first step in under- croorganisms has relied primarily on
maintain and improve microbiological standing foodborne pathogens has been structural (morphological) and func-
food safety. Control strategies that to develop a system of nomenclature and tional (physiological) characteristics.
descriptions of microorganisms within For example, shape is a morphological
were once effective may not remain so
this system. For the purposes of study, characteristic, and the pattern of en-
if the pathogens become tolerant. scientists try to classify microorganisms zymes produced is a physiological char-
Fortunately, genomic and improved based on a set of common characteristics acteristic. The commonly used morpho-
molecular and imaging techniques have that sometimes include presumed patho- logical distinctions of gram-positive and
vastly expanded scientific understanding genic attributes. However, as our scientif- gram-negative are based on differences
of the organisms that cause foodborne ic understanding has improved, the in cell wall composition. Morphological
disease. These tools also have enabled initial classifications often no longer features remain the primary means of
scientists to attribute foodborne disease present a full and accurate picture. When classification for molds. Although mor-
to microorganisms that had not previ- nomenclature becomes outdated, ques- phological characteristics can classify
ously been identified as pathogenic or as tions are raised about the scientific valid- bacteria into broad categories (e.g.,
foodborne. ity of regulatory policies based on classi- spherical, rod-shaped, or curved), bacte-
However, researchers still have many fication schemes that predict pathogenic- ria generally have few morphological fea-
questions to answer: What makes one
strain of a microbe pathogenic when
other microorganisms within the same
species are not? How do microorganisms Table 3. Classic Microbial Nomenclature
become pathogenic? Understanding Nomenclature Example 1 Example 2 Example 3
pathogenicity is not just necessary for
developing methods to treat illness but is Family Enterobacteriaceae Enterobacteriaceae Mycobacteriaceae
also needed for pathogen control. Genera/genus Escherichia Salmonella Mycobacterium
Pathogen control includes preven-
Species coli enterica avium
tion of food contamination, elimination
from the food, reduction to an acceptable Subspecies enterica paratuberculosis
level, or prevention of multiplication and Serovar O157:H7 Typhimurium
toxin formation. In addition, when sci-

safety management, many scientific dis- too must our management strategies and management framework should use food
ciplines contribute to our knowledge our regulatory framework. Regulatory safety objectives to translate data about
about food safety. The scientific commu- programs must be flexible to address is- risk into achievable public policy goals.
nity must pull together multidisciplinary sues as they arise and to benefit from sci- Microbiological food safety issues
teams that combine microbiology, epide- entific advances. Continued research will will continue to emerge. Although we
miology, genetics, evolutionary biology, improve our understanding of the com- cannot expect to accurately predict the
immunology and other areas of expertise plex factors that cause foodborne illness, details of complex changes such as
to enhance our understanding of the in- and surveillance programs will gather pathogen evolution, scientific knowledge
terrelated factors that drive emerging data to document the effectiveness of our can be used to identify the areas of great-
food safety issues. controls and identify new problems as est concern, so that we may be ready to
Just as the issues change over time, so they emerge. A science-based food safety respond as issues arise.

Science of Pathogenicity
Pathogenicity is the ability to cause entists understand how a particular ity poorly or that cluster pathogenic and
illness. Because pathogens are living pathogen is able to cause illness, then nonpathogenic microbes together under
they can look for ways to disrupt this one name.
organisms that rapidly adapt and
process and render the microorganism The names used to describe various
evolve, the methods they use to cause harmless or find treatments that mitigate microbiological foodborne pathogens
illness are never static. Pathogen illness. The very factors that create are based on systematic nomenclature. It
evolution is continuous and is driven pathogenicity are opportunities for con- is common practice to identify an organ-
trol. Just as the pathogens adapt and ism based on its genus and species. To
by a variety of forces, only some of evolve, so can our understanding and provide additional detail, classifications
which relate to human activities. The our response. such as subspecies, strain, serotype,
continual evolution of foodborne pathovar, and toxin type may be used
pathogens forces us to change food
Nomenclature (see Table 3).
In the past, the classification of mi-
production processes and products to Traditionally, the first step in under- croorganisms has relied primarily on
maintain and improve microbiological standing foodborne pathogens has been structural (morphological) and func-
food safety. Control strategies that to develop a system of nomenclature and tional (physiological) characteristics.
descriptions of microorganisms within For example, shape is a morphological
were once effective may not remain so
this system. For the purposes of study, characteristic, and the pattern of en-
if the pathogens become tolerant. scientists try to classify microorganisms zymes produced is a physiological char-
Fortunately, genomic and improved based on a set of common characteristics acteristic. The commonly used morpho-
molecular and imaging techniques have that sometimes include presumed patho- logical distinctions of gram-positive and
vastly expanded scientific understanding genic attributes. However, as our scientif- gram-negative are based on differences
of the organisms that cause foodborne ic understanding has improved, the in cell wall composition. Morphological
disease. These tools also have enabled initial classifications often no longer features remain the primary means of
scientists to attribute foodborne disease present a full and accurate picture. When classification for molds. Although mor-
to microorganisms that had not previ- nomenclature becomes outdated, ques- phological characteristics can classify
ously been identified as pathogenic or as tions are raised about the scientific valid- bacteria into broad categories (e.g.,
foodborne. ity of regulatory policies based on classi- spherical, rod-shaped, or curved), bacte-
However, researchers still have many fication schemes that predict pathogenic- ria generally have few morphological fea-
questions to answer: What makes one
strain of a microbe pathogenic when
other microorganisms within the same
species are not? How do microorganisms Table 3. Classic Microbial Nomenclature
become pathogenic? Understanding Nomenclature Example 1 Example 2 Example 3
pathogenicity is not just necessary for
developing methods to treat illness but is Family Enterobacteriaceae Enterobacteriaceae Mycobacteriaceae
also needed for pathogen control. Genera/genus Escherichia Salmonella Mycobacterium
Pathogen control includes preven-
Species coli enterica avium
tion of food contamination, elimination
from the food, reduction to an acceptable Subspecies enterica paratuberculosis
level, or prevention of multiplication and Serovar O157:H7 Typhimurium
toxin formation. In addition, when sci-

tures that are readily discernible by light food and clinical samples (King et al., Mining the sequences for the relative
microscopy or that are stable under a 1989). Although the use of rRNA se- “time” that specific segments appeared
broad range of environmental conditions. quences as a chronometer to measure re- within the genome revealed the reasons
To create a system with more precision, lationships among species has disrupted for the discordance: significant portions
taxonomists were forced to base classifica- traditional groupings based on pheno- of microbial genomes have been ac-
tion schemes on both morphological typic characteristics, many of the taxa of quired through gene transfer from other
characteristics and physiological charac- importance to food microbiology remain microorganisms (Lawrence and
teristics that generally reflect the biochem- intact, with some modifications among Ochman, 1998). Examining large sets of
ical diversity among bacterial species. groupings of certain species. For exam- virulence genes on contiguous segments
As the available techniques and tech- ple, Campylobacter pylori, initially of DNA (known as pathogenicity is-
nology advanced, scientists found new named pyloric campylobacter for its lands) also demonstrated that genes
ways to classify microorganisms. The ad- similarity to Campylobacter jejuni, was conferring virulence characteristics are
vent of ribosomal RNA (ribonucleic subsequently renamed Helicobacter py- often some of the most recent acquisi-
acid) sequencing began a new era of tax- lori (Dubois, 1995). tions among the genomes of pathogenic
onomy (Woese et al., 1990). rRNA is The era of microbial genomics species (Hacker and Kaper, 2000). Aside
present in organisms in all kingdoms reached full swing in the 1990s. Using from the impact on nomenclature, this
and performs the same essential func- several available microbial genome se- new information has profoundly
tions in all organisms. rRNA evolves quences, scientists have been able to com- changed scientific thinking about the
slowly so it serves as the ideal evolution- pare the evolutionary histories of different evolution of virulence. The ability of a
ary clock. Scientists soon developed large bacterial “races” (phylogenies) to the uni- pathogen to suddenly obtain a critical
databases of rRNA sequences used to versal phylogenetic tree predicted from virulence factor through genetic ex-
classify new species (Olsen et al., 1992). rRNA sequences. These efforts resulted in change is at odds with the idea of slow,
This era also produced many of the cur- the disappointing discovery that the ge- gradual evolution of virulence.
rent DNA (deoxyribonucleic acid) hy- nome-based phylogenies were frequently Now that scientists know that micro-
bridization strategies used to detect and discordant with rRNA predictions (Brown bial genomes change more rapidly than
identify pathogenic microorganisms in and Doolittle, 1997). previously believed, the concept of bac-

Nomenclature of
gastroenteritis (caused by S. Typhimu- cidence of typhoid fever is declining
Salmonella riuim, S. Enteritidis, and others); enter- (due, in part, to better distribution of
Bacteria in the genus Salmonella ic fever (S. Typhi and S. Paratyphi); and safe water and successful vaccines),
are important contaminants in food an invasive systemic disease (S. Choler- while the incidence of nontyphoidal
and water. Recently, efforts have been aesuis). In the United States, nonty- salmonellosis is increasing rapidly.
made to simplify the nomenclature phoidal Salmonella account for an esti- A portion of this increase correlates
of Salmonella. Instead of using sero- mated 1.3 million illnesses annually, to changes in the food production
type designations (of which there are with several hundred deaths (Mead et environment that may have given
more than 2,000) incorrectly as spe- al., 1999). The U.S. incidence of typhoid Salmonella the opportunity to spread
cies designations, most Salmonella fever is relatively low—approximately and to contaminate foods that are
species are now classified as Salmo- 700 cases annually, mainly as a result of distributed through large complex
nella enterica and then further iden- international travel. Worldwide, the in- networks.
tified by serovar (e.g., Salmonella ty-
phimurium becomes S. enteri-
ca serovar Typhimurium, see
Fig. 3). For convenience, the Fig. 3. Nomenclature of Salmonella
species (enterica) designation
Genus Salmonella
is frequently eliminated, leav-
ing Salmonella Typhimurium.
The diverse population of
organisms sharing the same Species enterica
name has complicated efforts
to study Salmonella, but re-
cent advances illustrate that Subspecies diarizoni salamai arizoni enterica houtenae indica bongori
most Salmonella are actually
quite similar to each other, es-
pecially at the virulence factor Serovar Enteritidis Typhi Typhimurium Paratyphi Choleraesuis
Salmonella typically cause
three diseases in humans:


terial “species” is in flux. In terms of di- Fig. 4. Virulence and Foodborne Illness different Salmonella sub-
versity, genome size may vary by 20% types certainly suggested
among subpopulations of a single spe- Number of that numbers >100,000
cies (for example, see Bergthorsen and Organisms cells were required for ill-
Ochman, 1998). This variability can Few Many ness (D’Aoust, 1985).
cover as many as 1-2 megabases of DNA High Severe/ However, outbreaks in-
that code for thousands of genes, which Many volving cheddar cheese
can confer unique characteristics—such and chocolate were ap-
as virulence—on specific subpopula- Virulence Severity of Illness/ parently caused by very
Number of Cases few cells (<10 total cells
tions. Still, a subset of genes that define
signature characteristics of the species for cheddar and 50-100
must be shared among all members of total cells for chocolate).
Low Few
that species. It has been theorized that
These contrasting views of what con- the lipid content of ched-
stitutes a bacterial species challenge the dar cheese and chocolate
concepts that underlie microbiological may cause only minor effects in a small facilitated the pathogen’s transit through
criteria and testing for the control of number of cases (less virulent). Viru- the stomach acid. Very little is known
pathogens in food manufacturing. In lence is related to the severity of disease about specific food matrices and the ef-
some cases, the potential to cause food- and the number of ingested pathogens fect on microbial survival and virulence.
borne disease can be characteristic of an (infectious dose) required to cause ill- Some salmonellae appear to be acid sus-
entire species, such as S. enterica, but in ness (see Fig. 4). Within the Escherichia ceptible, and others appear acid tolerant,
other cases it may be a consequence of coli species, for example, there is great but additional research will be required
recently evolved virulence characteristics contrast in virulence. Enterohemorrhag- to better answer this question. Antacid
among specific subpopulations of a spe- ic E. coli (e.g., O157:H7) can cause sig- consumption has been shown to affect
cies, such as Escherichia coli O157:H7. nificant and severe illness even if very the apparent virulence of certain patho-
The sensitivity of genome-based finger- small numbers of cells (10 or less) are gens such as Salmonella and L. monocy-
printing methods has even called into ingested, whereas enterotoxigenic E. coli togenes, and this suggests that stomach
question the equality of virulence in ge- require an estimated 100 million to 10 acid, and a microorganism’s tolerance to
netically distinct subpopulations of E. billion cells to cause a relatively mild set stomach acid, plays some role in defining
coli O157:H7 (Kim et al., 1999). As an- of symptoms (FDA/CFSAN, 2002). The the infectious dose.
other example, it is questionable whether underlying reasons for observed differ- Nowhere in current food microbiol-
all microorganisms in the Listeria mono- ences in virulence among various patho- ogy is the issue of infectious dose as
cytogenes species are capable of causing gens, and even within a single species of contentious as in the case of L. monocy-
disease in humans. Even though each pathogen is difficult to state with abso- togenes. Currently, the detection of L.
distinct genetic lineage of the species ap- lute certainty, as at least two dynamics monocytogenes in ready-to-eat foods is
pears to harbor the known virulence are operative, the microorganism and the grounds for removing the foods from the
genes, mounting phylogenetic evidence host. Even less virulent pathogens can marketplace. L. monocytogenes only very
indicates that virulence characteristics cause serious illness in debilitated hosts. rarely affects healthy individuals, but im-
differ (Rasmussen et al., 1995; Wied- Likewise, it is probable that fewer patho- mune-compromised individuals are sus-
mann et al., 1997). gens need to be ingested by a debilitated ceptible to illness and sometimes death.
New scientific information provides host than a healthy host to cause infec- Of all the known pathogens, L. monocy-
the opportunity to better target the tion if all else is equal. togenes has one of the highest mortality
pathogenic subpopulations within a spe- The infectious dose is different for rates, approaching 20% (Mead et al.,
cies. Present day approaches to control each pathogen. As stated above, E. coli 1999).
must be modified to be consistent with O157:H7 is infectious in very low num- The question is whether there is an
the information presently available. As bers. There may be several possible ingested dose of L. monocytogenes that is
improved detection and identification explanations for this, including: tolerable by the vast majority of the pop-
methods enable scientists to differentiate (1) O157:H7 is more acid tolerant and ulation (i.e., is there a realistic dose that
between virulent and avirulent organ- therefore fewer cells are killed by gastric can be tolerated in food?). Studies on vir-
isms, we should be able to allocate our acidity, (2) O157:H7’s virulence may be ulence gene and ribotype pattern have
risk management resources more effi- influenced by intestinal flora via quorum separated L. monocytogenes into three
ciently, focusing only on pathogenic or- sensing (see sidebar, p. 16), (3) its com- lineages, and each lineage appears to dif-
ganisms in our food supply. bined virulence factors simply make it fer in its pathogenic potential for hu-
more adaptable to the intestinal lumen, mans (Wiedmann et al., 1997). Studies
Virulence or (4) its virulence factors are more po- on L. monocytogenes isolated from
tent. smoked fish using the same methods fur-
If pathogenicity is a microorganism’s The situation among Salmonella is ther suggest that some subtypes of L.
ability to cause disease, then virulence more complex. Prior to the 1980s, con- monocytogenes in ready-to-eat foods may
can be considered the degree of pathoge- ventional wisdom held that large num- have limited pathogenic potential for hu-
nicity. Some pathogens are particularly bers of Salmonella were necessary for in- mans (Norton et al., 2001). If these vari-
efficient at causing clinically significant fection. Human feeding trials of volun- ations in pathogenic potential exist as
disease (highly virulent), while others teers from penal institutions with several suggested, it implies that more special-

Quorum Sensing toinducer. The terminology to describe tem in Shigella flexneri does not reg-
Not long ago, bacteria were these events is quorum sensing. ulate virulence. There may be
thought to lead a solitary existence Quorum sensing has been demon- sound ecologic reasons why some
and either live or die as a single cell. It strated in E. coli and Salmonella Typh- enteric pathogens regulate virulence
has been established that intercellular imurium (Surette and Bassler, 1998), with quorum sensing systems and
communication is fairly common and more recently, the role of quorum others do not. Quorum sensing sys-
among bacteria, and that this intercel- sensing in the virulence of enterohem- tems are not limited to the gram-
lular communication can lead to co- orrhagic (EHEC) and enteropathogen- negative bacteria, and notable gram-
ordinated activities once thought to ic (EPEC) E. coli has been elucidated positive bacteria, such as the patho-
be the exclusive domain of multi-cel- (Sperandio et al., 1999). The hallmark gen Staphylococcus aureus and its
lular organisms. It was not surprising intestinal lesion caused by EHEC and numerous virulence factors are un-
then that researchers asked whether EPEC is called attaching and effacing, der the control of intercellular sig-
intercellular communication was in- and is coded by the Locus of Entero- nals (de Kievit and Iglewski, 2000).
volved in virulence, and it was also cyte Effacement (LEE). This pathoge- Obviously it is important that
not surprising that genetically well nicity island codes for a type III secre- we gain a better understanding of
characterized foodborne pathogens tion system, as well as other virulence the regulation of virulence via quo-
such as Salmonella and Escherichia factors such as the intimin intestinal rum sensing systems. One obvious
coli would be investigated. colonization factor and the translocat- question is: Does quorum sensing
Intercellular communication ed intimin receptor protein. It is possi- occur in or on foodstuffs, and if so,
among bacteria is carried out by ble that the low infectious dose of E. is it a factor in the virulence of food-
small molecules called autoinducers. coli O157:H7 is in part because the borne pathogens? Many pathogenic
The theory is that at very low popu- pathogen is induced to colonize the in- bacteria have evolved a chemical
lation densities, there is insufficient testine by quorum sensing of signals language, and it would behoove us
autoinducer in the environment to from resident, nonpathogenic E. coli in to learn and understand that lan-
be detected by those bacteria present, the intestine of the host. guage. It may be possible to exploit
but that when some “threshold” Quorum sensing appears to regu- these intercellular communication
number of bacteria is reached, auto- late the virulence factors of a wide vari- pathways to reduce virulence, or use
inducer is present in sufficient con- ety of plant and animal pathogens them as targets of novel antimicro-
centration to trigger some activity in (Day and Maurelli, 2001). Unlike oth- bial substances (de Kievet and Ig-
bacteria capable of detecting the au- er enteric pathogens, the signalling sys- lewski, 2000).

ized testing might be prudent before functional virulence factors will dictate Toxins are perhaps the best under-
foods are rejected for the presence of L. which host a pathogen will colonize, stood family of bacterial virulence fac-
monocytogenes that may not be patho- which tissues will become infected, and tors, presumably because they are often
genic. ultimately which disease symptoms will secreted into the area surrounding the
The inherent ability to cause disease occur. bacteria where they can be isolated and
is the result of virulence factors encoded Many bacterial pathogens are genet- studied. Toxins have specific mechanisms
at the genetic level (Finlay and Cossart, ically similar to common bacteria that to recognize host cell surface receptors
1997; Finlay and Falkow, 1997). Many inhabit the host but do not cause dis- enabling them to transport themselves
diverse characteristics are considered vir- ease under ordinary circumstances into the host cell. Some toxins can mod-
ulence factors. If these factors are miss- (commensal organisms). Thus, a ify specific cellular targets to affect fluid
ing, the microorganism would be expect- pathogen is often a “genetically en- secretion, cytoskeletal structure, or even
ed to be less virulent or avirulent. Some hanced” organism: a common organ- nerve functions. Others insert them-
examples of virulence factors include: ism that contains a specialized collec- selves into the host cellular membrane,
• toxins (molecules secreted by the tion of virulence factors. This compli- resulting in cell disintegration or disso-
bacteria that affect host cell processes), cates efforts to control foodborne lution (lysis). Despite the vast number
such as cholera toxin; pathogens by diffusing resources across of cellular targets, toxins can be classified
• adhesins (molecules that enable a large group of microorganisms when into families based on their structure
pathogens to adhere to host surfaces), only a subset can cause foodborne ill- and function.
such as fimbriae; and, ness. The ability to share the genetic To cause disease, most pathogens re-
• invasins (molecules that enable material that encodes virulence factors quire the ability to adhere to host surfac-
pathogens to actively enter into a host within food-producing animals, the en- es following ingestion. Mammalian
cell (invasion) where they can exist as an vironment, or the human gastrointesti- hosts have several nonspecific defenses
intracellular pathogen), such as those nal system significantly complicates designed to prevent colonization by in-
used by Shigella and Salmonella. control (see Evolution, p. 19). Each of hibiting pathogen attachment, such as
Most pathogens have a variety of vir- the several steps in the progression of peristalsis, the mucocilliary system, and
ulence factors that assist in host coloni- pathogenic foodborne disease requires even cell sloughing (see section on hu-
zation and disease. The repertoire of one or more virulence factors. man host, p. 28). Bacterial pathogens


have a wide variety of adhesins, usually pathogen with additional environments host defenses such as antibodies, it also
glycoproteins or glycolipids, on their sur- to colonize that protect the pathogen exposes the pathogen to another mecha-
face that target specific host cell mole- from host defenses present within the lu- nism that kills most bacteria: fusion
cules. These adhesins are usually fila- men of the intestinal tract. The virulence with the lysosome. Lysosomes are small
mentous- or hair-like structures (fimbri- factors that facilitate invasion may be as sacks within the cell that contain en-
ae or pili) or proteins without the hair- simple as a single surface protein, such as zymes that “digest” substances—such as
like fimbriae (afimbrial adhesins) on the those used by Yersinia (invasin) or Liste- old DNA, proteins, or lipids—into small
bacterial surface. Pathogens usually en- ria (internalin). In other cases, the fac- pieces for reuse by the cell. Invasive
code several adhesins that help dictate tors may be complex, requiring the deliv- pathogens, including bacteria and pro-
tissue and host specificity. For example, ery of several proteins into the host cell tozoan parasites, have devised several
Salmonella use a combination of at least and resulting in profound cell surface strategies to avoid lysosomal fusion fol-
six different adhesins that contribute to changes such as membrane ruffling and lowing invasion. For example, a second
intestinal colonization. Many pathogens macropinocytosis before bacterial uptake Type III secretion system alters the tar-
also have the ability to adhere to the area occurs. geting of the membrane-bound vacuole
outside and surrounding the cell (extra- Numerous bacterial pathogens, in- surrounding Salmonella, causing the
cellular matrix), which contributes to cluding Salmonella and Shigella, have a vacuole to diverge from the standard
host colonization. Recently, it has be- complex secretion apparatus, known as a pathway that would deliver it to a lysos-
come apparent that some pathogens, Type III secretion system, that delivers ome. The salmonellae then live in the
such as E. coli O157:H7, actually insert numerous bacterial proteins into the gel- protected intracellular environment of
their own receptor into host cells, which like fluid inside the host cell (cytosol) to the vacuole (see sidebar below). In con-
then enables them to adhere to the out- mediate invasion. Type III secretion sys- trast, Shigella and L. monocytogenes use
side surface of the host cell (Kenny et al., tems are major virulence mechanisms enzymes to degrade the vacuolar mem-
1997). for many gram-negative pathogens brane, thereby releasing the pathogen
Many foodborne pathogens have the (Hueck, 1998). Salmonella actually have into the host cytosol. Once present in
additional capacity to invade host cells. two systems (one for invasion, one for the cytosol, the pathogens use the struc-
For example, Salmonella, Shigella, Yersin- intracellular survival), while Yersinia use tural proteins in the cell around them to
ia, and Listeria are invasive organisms, one to avoid isolation and destruction propel themselves within the cell and
capable of penetrating the intestinal epi- within the cell (phagocytosis). into a neighboring cell. Finally, patho-
thelial barrier as part of their pathoge- Although invasion into a host cell gens such as Yersinia and enteropatho-
nicity. The ability to invade provides the may protect the pathogen from some genic E. coli use their Type III systems to

Virulence of about the mechanisms Salmonella use to virulence plasmid that provides the
enter epithelial cells. These intestinal factors needed for prolonged survival
Salmonella cells are not phagocytic, and thus do not within the host.
Recently, scientists have made sig- normally ingest microorganisms. How- S. Typhi is different from most S.
nificant advances toward understand- ever, Salmonella use a Type III secretion enterica serovars in that it has a capsule
ing the molecular mechanisms of the system to inject several bacterial factors and does not encode the virulence
pathogenicity of Salmonella. Similar into the host cell. These molecules affect plasmid. Because of its systemic infec-
to pathogenic E. coli, Salmonella have normal cellular processes, including tious nature, S. Typhi presumably has
a collection of virulence factors, in- those that control the actin cytoskeleton additional virulence factors that con-
cluding factors needed to adhere to and other signal transduction pathways. tribute to the different nature of the
intestinal surfaces, invade host epithe- The end result is significant actin rear- disease. Although Salmonella species
lial cells, and survive within phago- rangement beneath the adherent bacteri- are fairly close relatives of E. coli, they
cytic cells. It has been estimated that um, membrane ruffling, macropinocyto- have many additional genes that pre-
Salmonella contain more than 200 sis, and engulfment of the bacterium into sumably account for their virulence.
virulence factors, encoded in at least a membrane-bound vacuole. Unlike Scientists know little about the role for
five pathogenicity islands in addition Shigella, Salmonella remain within the most of these additional genes and the
to a virulence plasmid and many vacuole to survive and proliferate. Sal- factors they encode.
pathogenicity islets. monella redirect vacuole movement Significant progress has been made
The complex mechanisms used within the host cell so that the vacuole it with vaccines for S. Typhi. Two current
by Salmonella species to adhere to inhabits does not fuse with lysosomes. vaccines—one live-attenuated strain,
intestinal cells continue to be studied Salmonella also form specialized the other a component vaccine—have
and debated. Many adhesins have structures that enable it to survive and significantly decreased the levels of ty-
been reported, and because they replicate within phagocytic cells. Salmo- phoid fever worldwide. However, little
appear redundant, defining the role nella species have another Type III secre- success has been made toward control-
of each in the disease process has tion system that encodes several factors ling nontyphoidal salmonellae, which
been difficult. needed for survival in this intracellular continue to cause increasing numbers
Significantly more is known compartment. Finally, Salmonella have a of illnesses worldwide.

avoid being pulled into the cell and regulated by a variety of control mecha- The continual genetic exchange be-
therefore blocking phagocytosis, allow- nisms and regulatory circuits. Successful tween bacteria ensures that pathogens
ing them to remain attached to the exte- pathogens are very adept at sensing their will continue to evolve as they acquire
rior of the cell (extracellular pathogens). microenvironment, and virulence factor different combinations of virulence fac-
Because expression of virulence fac- expression often relies on environmental tors. This evolution is a natural process,
tors at the correct time and place is criti- parameters to ensure coordination and although it can be enhanced and facili-
cal, bacterial virulence factors are tightly appropriate expression. tated by human actions.

Pathogens Are More ally present in low numbers does not en- tions to sporulate and become infectious.
sure product safety, as the infectious doses Since 1981, enteric protozoa have be-
Than Just Bacteria (100-102 infectious units) are presumed to come the leading cause of waterborne dis-
be low (Iversen et al., 1987; Jaykus, 2000b; ease outbreaks for which an etiological
Although bacteria are perhaps Moe et al., 1998). agent could be determined (Moe, 1996).
the first type of microorganism that Three major routes for viral contam- Although considerably less information is
come to mind when discussing mi- ination of foods have been recognized available about their importance in food-
crobiological food safety, they are by and include: (1) shellfish contaminated borne disease, their potential for trans-
no means the only pathogenic food- by fecally polluted marine waters; mission by foodborne routes is increas-
borne microorganisms. (2) human sewage pollution of drinking ingly recognized (Bean et al., 1990). For
and irrigation waters; and (3) ready-to- instance, from 1988-1992, seven food-as-
Human Enteric Viruses eat and prepared foods contaminated as sociated outbreaks of giardiasis, compris-
a result of poor personal hygiene of in- ing 184 cases, were reported in the United
Viruses of concern to human fected food handlers (Jaykus, 2000b). In States (Bean et al., 1996), and protozoan
health that are known to be transmis- addition, the NLVs have been shown to parasites such as Giardia and Cryptospo-
sible through foods are shed in the fe- be spread by aerosolization of vomitus ridium species may be present in shellfish-
ces of infected humans and transmit- and through fomites (Marks et al., 2000; growing waters as a result of contamina-
ted via the fecal-oral route. Of these Patterson et al., 1997). tion with animal farm runoff or as a re-
viruses, hepatitis A virus causes the sult of treated and untreated sewage in-
most serious recognized foodborne Protozoan Parasites put. The ability of bivalve molluscs to
viral infection, whereas the Norwalk- concentrate Giardia and Cryptosporidium
like gastrointestinal viruses (NLVs) Like viruses, parasitic protozoa repli- has been demonstrated by Toro et al.
are the most prevalent. According to cate in the intestines of infected hosts (1995). Cryptosporidium oocysts have
recent epidemiological estimates, the and are excreted in the feces. However, been isolated in Eastern oysters harvested
NLVs account for over 60% of cases, their host range is wider than viruses, be- from commercial sites in the Chesapeake
33% of hospitalizations, and 7% of ing able to replicate in human and non- Bay (Fayer et al., 1998).
deaths among all of the illnesses that human animal hosts. Since they are The most common human enteric
are attributable to known foodborne transmitted primarily by the fecal-oral parasitic infections in the United States
pathogens (Mead et al., 1999). Hu- route, the major source of contamina- are caused by Cryptosporidium parvum
man enteric viruses have properties tion for foods and water is through con- and Giardia lamblia. Cyclospora is also
that make them quite different from tact with human and animal fecal pollu- an emerging enteric protozoan that has
the common bacterial agents of food- tion. This contamination may occur di- recently been associated with the con-
borne disease. As obligate intracellu- rectly, through contaminated meat car- sumption of contaminated fruits (Ortega
lar parasites, they require live mam- casses or poor personal hygiene practices et al., 1993). Large, community-wide
malian cells to replicate. To protect of infected food handlers, or indirectly, waterborne outbreaks of parasitic proto-
the viral genome from inactivation via contact with fecally contaminated zoa are usually associated with surface
outside of infected cells, virus parti- waters or other cross-contamination water supplies that are either unfiltered
cles have properties that make them routes. Like the viruses, the parasitic or subjected to inadequate flocculation
environmentally stable to the ex- protozoa (in the cyst or oocyst form) are and filtration processes (Moe, 1996).
tremes of pH and enzymes present in environmentally inert, they do not repli- Two large waterborne outbreaks have oc-
the human gastrointestinal tract. cate in foods, are extremely environmen- curred in the United States within the
This stability enables virus particles tally stable, resistant to many of the tra- last 10 years (Hayes et al., 1989; MacKen-
to survive a variety of food produc- ditional methods used to control bacteri- zie et al., 1994), including the largest re-
tion, processing, and storage condi- al pathogens, and have notably low infec- corded waterborne disease outbreak in
tions making virtually any type of tious doses (DuPont et al., 1995; Haas, U.S. history (MacKenzie et al., 1994).
food product a potential vehicle for 1983). Although transmitted by the fecal-
transmission of viral pathogens oral route, direct person-to-person Marine Biotoxins
(Jaykus, 2000a). The inability of hu- transmission of parasitic protozoa is un-
man enteric viruses to replicate in likely because excreted oocysts require Marine biotoxins are produced by
foods and the fact that they are gener- days or weeks under favorable condi- several dinoflagellate and diatom spe-


Although foodborne pathogens have and how it overcomes host defenses and ploited for potential therapeutics and
developed a vast repertoire of virulence causes illness creates opportunities for control strategies.
factors, several common themes enable preventing the infection or for mitigating
scientists to place many of these factors the illness. The use of similar kinds of Evolution
in related families based on structure, Type III secretion systems among many
function, and other characteristics. Un- diverse pathogens is one example of a Pathogen evolution is a continuous
derstanding why a pathogen is virulent common mechanism that might be ex- biological process that is influenced by

cies (Epstein, 1998; Plumley, 1997), upon consumption (Baden et al., 1995). In general, except when large
most of which are produced by the pro- Symptoms of seafood-borne intoxica- numbers of people are affected, medi-
liferation of algae in the form of harm- tions may include gastrointestinal dis- cal professionals are unlikely to rec-
ful algal blooms (HABs) (Steidinger tress, vomiting, headaches, neurologic ognize mycotoxicoses because of in-
and Penta, 1999). Of the several thou- dysfunction, paralysis and muscular sufficient knowledge about these dis-
sand identified marine microalgae, at pain. The degree of human toxicity is eases and the lack of appropriate di-
least 80 species are known to be toxic or affected by the health of the victim, the agnostic methods. Unlike microbial
harmful (Baden et al., 1995). Reports of amount of toxin ingested, the rate of agents that can be detected by culturing
seafood toxicity due to these biotoxins toxin elimination, and the biotransfor- and/or PCR amplification, mycotoxins
date back to the 1600s, have occurred mation of toxins by enzyme systems are metabolized and may no longer be
worldwide, and recent evidence suggests within the body (Steidinger and Penta, present in the tissues of patients
that HABs are increasing. This indi- 1999). shortly after the onset of acute
cates that marine biotoxins may indeed disease.
be considered emerging pathogens Mycotoxins Mycotoxins produced by a wide
(Anderson, 1994; Shumway, 1989). variety of molds including Aspergil-
The toxins produced by dinoflagel- A large group of mycotoxins, known lus, Penicillium and Fusarium may
late and diatom species are often classi- collectively as trichothecenes, have been cause chronic toxicosis (Coulombe,
fied according to their mode of action associated with acute human illness 1993). Chronic effects often result
and resulting disease syndromes. The (Pestka and Casale, 1990). The most se- from prolonged ingestion of low to
most common marine HAB toxins are vere manifestation is alimentary toxic moderate levels of toxin that do not
chemically characterized as alkaloids, aleukia. Initial symptoms after a single produce symptoms of an acute illness,
polyethers, or substituted amines and contaminated meal include throat in- making the chronic effects difficult to
are the end products of elaborate bio- flammation, vomiting, diarrhea and ab- attribute to contaminated food. The
chemical pathways (Plumley, 1997). dominal pain; with continued ingestion, link between aflatoxin and human liv-
Most have been classified as neurotox- the illness can progress to oral hemor- er cancer has been well established
ins although some hemolytic substances rhaging, pneumonia, bone marrow de- through the use of clinical biomarkers
have also been identified (Baden et al., pletion, and potentially death. Human (aflatoxin adducts), but other organs
1995). Although marine toxins are outbreaks of gastrointestinal illness have (kidney, spleen and pancreas) also
pharmacologically diverse, most exert been linked to millet contaminated by a may be affected. Another chronic dis-
toxic effects through perturbations of variety of Fusarium that was capable of ease link that has been the subject of
voltage-gated sodium channels located producing T-2 toxin and other trichoth- considerable study is those diseases
in excitable membranes of neurons ecenes and also wheat and barley infect- induced by the fumonisins, zearale-
(Catterall, 1985; Manger et al., 1995). ed with Fusarium that produced the tri- none, and trichothecene mycotoxins.
Binding of these toxins to receptor sites chothecenes deoxynivalenol (vomitoxin), Fumonisin levels in corn-based foods
leads to conformational changes of the nivalenol and fusarenon-x (Bhat et al., have been statistically associated with
ion pore of the channel, thus altering 1989; Luo, 1994). an increased risk of human esoph-
the flow of ions controlling nerve sig- Other mycotoxins have been associ- ageal cancer. Zearalenone has been
naling (Baden et al., 1995). ated with acute disease. Aflatoxin inges- associated with premature puberty.
In general, the marine biotoxins are tion has caused acute liver inflamma- Trichothecenes modulate immune
small, chemically complex, and highly tion in Kenya (Ngindu et al., 1982) and function, meaning that over time
potent substances that tend to accumu- India (Krishnamachari et al., 1975). In mycotoxicosis could reduce immune
late in finfish and/or shellfish. When the early 20th century, cardiac beri- resistance to infectious diseases, facil-
the seafood is consumed by humans, it beri—an acute cardiac disease that pro- itate tumor growth through reduced
acts as a passive carrier of the toxins. duces a rapid pulse, abnormal heart immune function and cause autoim-
The toxins are tasteless, odorless, and function, and low blood pressure lead- mune disease (Bondy and Pestka,
most often heat and acid stable, which ing to respiratory failure and death— 2000; Jackson et al., 1996). Ochratoxin
means that routine food safety inspec- that occurred in Japan and other Asian A is becoming closely linked to the
tion and food preparation techniques countries was linked to contaminated kidney disease Balkan endemic neph-
will not detect contamination, inactivate rice containing the mycotoxin citreovir- ropathy as well as tumors in the uri-
the toxins, or prevent human disease idin (Ueno, 1974). nary tract and kidney.

environmental factors. Historically, sci- pletely different pathogenicity island Fig. 6. Genetic Material in E. coli
entists thought that pathogens arose inserted at exactly the same site
from sequentially cumulative muta- (Hacker et al., 1997), which encodes E. coli O157:H7 Nonpathogenic
E. coli
tions, gradually changing from avirulent an adhesin (P fimbriae) and a toxin
to pathogenic. In the past few years, (hemolysin), virulence factors need-
new evidence has shown that evolution ed for urinary tract colonization.
of pathogenicity progresses in quantum Yersinia and Shigella species encode
leaps that are driven by acquisition of Type III systems on their virulence
foreign DNA (see Fig. 5). Analysis of plasmids rather than in their chro-
some pathogen genomes has supported mosomal DNA, but they have other
this new understanding and even ex- virulence attributes that are chro-
tended it by demonstrating that genetic mosomal and not in islands. In ad-
exchange plays a larger role than previ- dition to pathogenicity islands,
ously thought in genome composition. smaller pieces of DNA (pathogenici-
Comparing genomes of related patho- ty islets) also appear to move be-
gens reveals many recently acquired tween bacterial pathogens.
genes scattered throughout the genome. Bacteriophages, viruses that in-
As discussed above, the ability to fect bacteria, also play a major role Shared genetic material
cause disease is attributed to specific vir- in the movement of virulence factors (4.1 million base pairs)
ulence factors. The genes encoding between pathogens. For example,
these virulence factors are often found Shiga toxin is a key virulence factor Genetic material only in E. coli O157:H7
on pathogenicity islands, that is, clus- for Shigella dysenteriae, which causes (1.37 million base pairs)
tered together at specific loci on the dysentery. The genes for toxin pro-
Genetic material not in O157:H7
chromosome or plasmids (Hacker et al., duction are encoded on a phage that
(0.53 million base pairs)
1997). Evidence indicates that these ge- has been incorporated into the chro-
netic regions have evolved independent mosome. E. coli O157:H7 also con-
of the rest of the microbe’s genetic in- tains genes for Shiga-like toxin(s), which
formation, i.e., they developed in a dif- cause hemorrhagic colitis and contribute ready possess an essential adhesin, thus
ferent organism and were acquired as a to disease progression to hemolytic ure- ensuring virulence.
set. These genetic regions usually have a mic syndrome, sometimes characteristic Genomics has greatly facilitated our
different G+C content of DNA, often of infection with this pathogen (Kaper understanding of pathogen evolution.
have repetitive ends, and are often in- and O’Brien, 1998). It is thought that the For example, comparing the recently
serted into or near tRNA genes. Particu- phage encoding this toxin infected an sequenced E. coli O157:H7 genome to a
lar pathogenicity islands encode specific EPEC strain of E. coli and created a new nonpathogenic E. coli reveals some sur-
virulence factors that in turn dictate pathogen, an EHEC. Under certain cir- prising information (Perna et al., 2001).
which disease the pathogen may cause. cumstances, the phage DNA replicates As expected, both strains share a com-
In gram-negative bacteria, Type III and breaks out, forming a new phage mon genetic “backbone” of about 4.1
secretion systems are often encoded and releasing the toxin. Another example million similarly arranged base pairs
within these pathogenicity islands. For of the role that phage play in the evolu- (see Fig. 6). However, the O157:H7 ge-
example, enteropathogenic (EPEC) and tion of pathogens is found within Vibrio nome contains an additional 1,387 new
enterohemorrhagic E. coli (EHEC), cholerae (Waldor and Mekalanos, 1996). genes in 1.37 million base pairs. Fur-
which both cause diarrhea, contain the The cholera toxin is encoded within a thermore, the nonpathogenic E. coli has
Locus of Enterocyte Effacement (LEE) bacteriophage capable of moving be- 0.53 million base pairs (528 genes) that
island, which encodes a Type III system tween strains, and, in this case, the recep- are not in O157:H7. Perhaps the most
and other virulence factors essential for tor for this phage is one of the pathogen’s significant finding is that the additional
disease (McDaniel et al., 1995). Howev- major adhesins (a pilus). This arrange- DNA in the pathogenic E. coli is distrib-
er, uropathogenic E. coli (which cause ment ensures that the phage encoding uted among 177 different packets, each
urinary tract infections) have a com- the toxin only infects bacteria that al- of which was likely inherited through
an independent event. Researchers cal-
culated that these two E. coli strains
Fig. 5. Contrasting Views of Pathogen Evolution shared a common ancestor approxi-
mately 4.5 million years ago. Although
Gradual evolution scientists know the function of two
pathogenicity islands (the LEE and the
Shiga toxin phage) within O157:H7 that
Avirulent Moderately virulent Highly virulent encode virulence factors, the function
of the additional genes within O157:H7
Genetic exchange remains to be determined, as does their
of virulence factors contribution, if any, to virulence. Even
Type III secretion Toxin-production among O157:H7 strains, significant
system acquired gene acquired variability in virulence can be detected,
indicating that genome diversification


Evolution of Salmonella other foodborne pathogens continues to serious gastroenteritis, the occur-
S. enterica shows significant diver- increase. In some Asian countries, more rence of quinolone-resistant Salmo-
sity in its host specificity, but the rea- than 90% of Salmonella isolates are re- nella in animals is a great concern.
sons for host specificity remain unde- sistant to the most commonly used hu- Although the genomic sequenc-
fined. Some serovars, such as S. Typhi, man antibiotics. Globally, the three main es of S. Typhimurium and S. Typhi
are very human specific while others causes of antimicrobial resistance have have been recently completed, sci-
are animal specific (e.g., S. Pullorum been identified as use of antimicrobial entists still have more questions
infects chickens). Others, such as S. agents in agriculture, overprescribing by than answers about Salmonella. It
Typhimurium and S. Enteritidis, have physicians, and misuse by patients. The is not known how they cause diar-
a wide host range. S. Typhimurium combination of increased antibiotic re- rhea, or why some are constrained
typically causes a diarrheal disease in sistance and an apparent increase in vir- by host specificity. Because of the
humans, but a typhoid-like disease in ulence has resulted in strains, such as S. complexity of their virulence fac-
mice. Because many strains of Sal- Typhimurium DT104, that continue to tors, little progress has been made
monella cannot tolerate the low pH of cause much concern. S. Typhimurium in converting the available knowl-
the gastric environment, the infec- DT104, which has a broad host reservoir, edge into therapeutics. Good agri-
tious dose for ingested exposure to is usually resistant to five antibiotics (i.e., cultural and manufacturing prac-
Salmonella is usually (but not always) ampicillin, chloramphenicol, streptomy- tices, appropriate food handling,
quite high (greater than 100,000 bac- cin, sulphonamides, and tetracyclines) and adequate water treatment
teria required to produce illness). and can be resistant to others (e.g., fluo- remain our best preventive mea-
However, if delivered intravenously, a roquinolones). Reporting on an out- sures for most Salmonella infec-
mere 10 organisms of strains that re- break of quinolone-resistant S. Typh- tions, although the typhoid vac-
quire a large oral infectious dose can imurium DT104, Molback et at. (1999) cines are effective against S. Typhi
kill a mouse. stated that because fluoroquinolones re- in humans, and vaccines for several
The incidence of antibiotic resis- main a standard treatment for suspected other serovars have shown promise
tance among Salmonella and some extraintestinal Salmonella infections and in food animals.

occurs rapidly. overlaid on a common genetic backbone. O26:H11/O111:H8 lineages of enterohe-

Genetic exchange between bacterial Also, many avirulent bacteria can carry morrhagic E. coli demonstrate that ac-
species is obviously frequent and can sig- inactive forms of genes common to viru- quisition of the same virulence gene ele-
nificantly affect the evolution of patho- lent strains. ments has occurred on multiple occa-
gens. The acquisition and spread of an- sions, even through parallel paths (Reid
tibiotic resistance has been an easy way Selection et al., 2000). This discovery raises a sig-
to follow genetic exchanges, and the effi- nificant question regarding the selective
ciency of this spread is demonstrated by Evolution and selection are closely pressures that cause the abrupt rise to
the pervasiveness of resistance in many related. Evolution produces microor- dominance of particular virulence gene
bacteria not previously resistant to anti- ganisms that are distinctly different combinations within a species.
biotics. As discussed above, the genetic from previous generations; selection In infectious diseases that are pri-
material that encodes virulence factors gives these mutant strains an advantage marily carried by humans and trans-
can move between bacteria, with the po- and causes them to become prominent. mitted person-to-person, the appear-
tential to rapidly create a new pathogen, Together, these forces have a profound ance of new alleles of virulence genes is
even from a commensal organism. A impact on the emergence of foodborne associated with the rise and spread of
major unanswered question is often pathogens. more virulent clones (Musser, 1996).
where these virulence factors originated. The proposed step-wise model (Feng This process likely also occurs among
Despite the prevalence of Type III secre- et al., 1998) for evolution of E. coli foodborne pathogens. However, food-
tion systems within several bacterial O157:H7 (as opposed to a gradual evo- borne pathogens must overcome
pathogens, scientists have not found the lution) points out some rather interest- unique hurdles, including survival in
system’s ancestor. ing features of the process by which new the pre-harvest environment, as well as
As in all organisms, the evolution of pathogens emerge. First, mobility of survival during food processing, stor-
pathogens is continuous. In some cases, gene segments appears to be a limiting age, and preparation.
classifying pathogens based on their vir- factor in the rate at which microorgan- Many of the hurdles in food pro-
ulence factors is a more logical method isms can test new gene combinations. duction and processing are a different
than classification based on serotype or New high-throughput genome sequenc- set of selective pressures than those ex-
some other trait unrelated to virulence. ing methods will produce data to develop erted by the human host’s gastrointesti-
The evolution of pathogens will become a much better estimate of the frequency nal tract. Successful foodborne patho-
clearer as scientists sequence and study of such events and an improved under- gens, such as Salmonella and L. monocy-
additional genomes of related species. standing of their underlying mecha- togenes, have acquired not only viru-
However, even seemingly related organ- nisms. Second, the common virulence lence characteristics, but also physiolog-
isms can contain significant diversity genes shared by the O157:H7 and EHEC ical and ecological characteristics that

allow them to propagate in food pro- posed during food production and tage conferred. The combination of ge-
duction and processing environments processing affect the emergence of new nomics and population genetics will pro-
and overcome hurdles. Using the new pathogens. However, hurdles imposed vide methods for identifying genetic al-
tool of genomics, researchers are exam- in food processing—such as pH, os- terations that correlate with the descent
ining how changes in food production, molarity, and temperature—are all of specific populations of foodborne
processing, storage, and preservation known to affect physiological charac- pathogens. However, scientists must be-
methods can impose new selective pres- teristics and, in some cases, virulence gin to devise strategies for identifying
sures on foodborne microorganisms characteristics of pathogenic microor- which genetic alterations, among the
and how such pressures might affect ganisms. A good model from which to many different gene sequences that de-
virulence in known pathogens or emer- begin drawing conclusions might be to fine a subpopulation, confer selective ad-
gence of new pathogens. examine the distribution of Shiga tox- vantage. Identifying and understanding
in-converting phages among strains of these genes may enable scientists to pin-
Shifts in Known Pathogens E. coli. Clearly, the Shiga toxins play a point the selective forces at work.
pivotal role in the pathogen’s ability to
A cause-effect relationship has been cause illness. However, Shiga toxin- Stress
documented between changes in food producing E. coli (STEC) can be found
production methods and shifts in popu- in many environments, and only cer- Each microbe prefers a specific set
lations of a pathogenic species favored in tain serotypes of STEC appear to com- of environmental conditions. When en-
the food production environment. Per- monly cause disease in humans, indi- vironmental parameters are significant-
haps the best example is the displace- cating that the Shiga toxins alone are ly different from the desired range, the
ment of Salmonella serovar Gallinarum insufficient to confer virulence. The microbes undergo stress. To be more
by the Enteritidis serovar in poultry pro- convergence of Shiga toxin genes and specific, stress is defined as chemical or
duction environments. Scientists theorize genes conferring other virulence char- physical parameters that impair the
the shift was caused by programs to acteristics—such as the ability to at- function of the macromolecular ma-
eradicate S. Gallinarum, a poultry patho- tach to host cells—is necessary for the chinery of the microorganism. Exam-
gen (Bäumler et al., 2000). Combina- emergence of a new and successful ples of stress for certain microorgan-
tions of mathematical modeling, epide- pathogen. Considering the hurdles im- isms might include high and low tem-
miologic investigations, and population posed in the food production and pro- perature, acidic pH, low water availabil-
genetic studies suggest that the popula- cessing environment, it seems likely ity, and presence or absence of oxygen.
tion shift and spread of S. Enteritidis that convergence of such genes onto Specific genes are activated, producing
took independent but parallel paths in physiologically robust genome back- proteins that protect the bacterium from
Europe and North America. Genetically bones favored the spread of EHEC lin- stress. This process, known as an adap-
distinct subpopulations of S. Enteritidis eages. Research is needed to identify tive response, improves the microorgan-
rose to dominance on the two conti- how selective pressures in the food ism’s ability to survive under the stress-
nents, in theory, due to competitive ad- production and processing environ- ful conditions. Although the responses
vantages over S. Gallinarum in occupy- ment affect the potential for new improve the range of conditions the mi-
ing the poultry environment (Rabsch et pathogens to emerge or for subpopula- croorganisms can tolerate, these re-
al., 2000). tions of known pathogens to increase sponses also require energy, so they are
Although this displacement likely did in dominance. only expressed when needed. Under
not involve biological changes in the By focusing on the results of selec- normal conditions, bacteria that do not
poultry host, it illustrates the capacity for tion in recently emerged foodborne turn off their stress responses would be
changes in veterinary practices to have pathogens, scientists can begin to ad- outgrown by those that reroute that en-
significant impact on the populations of dress these issues. The approach is an ergy to other cellular processes. Stress
microbial species that inhabit the pro- adaptation of the method used by ge- responses are of particular interest in
duction environment. In addition, it neticists to identify the genes involved foodborne pathogens because they can
demonstrates that such population shifts in a particular biochemical pathway. render bacteria tolerant to traditional
have the potential to change the relative First, scientists induce mutations at food processes or the intrinsic parame-
risk of foodborne illness to humans. random, and mutants of interest are ters of the food.
Bioinformatics uses computational selected based on phenotypic traits. Bacteria have evolved elaborate net-
methods to analyze large sets of biologi- Mutations that block the pathway un- works to protect against or repair dam-
cal data, such as genome sequences, or to der study are traced back to specific age caused by detrimental conditions.
make predictions, such as protein struc- genes. Once the genes are marked and Bacterial responses to stress are varied
tures. Given the tools of genomics and identified, scientists use biochemical and complex, including both structural
bioinformatics, it may be possible to un- and molecular techniques to under- and physiological changes. For most
derstand why such shifts occur when epi- stand how the genes function in the bacteria, these responses are modulated
demiologic studies fail to identify the ac- pathway. by specific sigma (F) factors (Grossman
tual selection pressure. In the case of foodborne pathogens, et al., 1984; Lange and Hengge-Aronis,
the strategy is similar but reversed. Here, 1991) or regulators (Christman et al.,
Emergence of New Pathogens the goal is to identify the genes or alleles 1989) that direct the activation of specific
that have been selected in food produc- genes that comprise regulons (large
Scientists know relatively little tion environments, elucidate their func- numbers of coordinately controlled
about how the microbial controls im- tion, and pinpoint the selective advan- genes) and encode for the proteins re-


sponsible for cellular protection. The complex system; more than 50 genes in fects of heat, and, as noted above, results
proteins produced in response to stress E. coli are responsible for its GSR and in cross protection to other stresses. In E.
enhance bacterial survival in the envi- are coordinately regulated by the prod- coli, a second heat shock system, con-
ronment outside the host, including in uct of the rpoS gene encoding Fs, an al- trolled by FE (F24), also has been identi-
foods (Cheville et al., 1996; Humphrey et ternative sigma-subunit of RNA poly- fied (Erickson and Gross, 1989, Wang
al., 1993; Jenkins et al., 1988; Leyer and merase (Loewen et al., 1998). Many of and Kaguni, 1989). This system recently
Johnson, 1993; Miller and Kaspar, 1993; the genes in the GSR regulon appear to has been shown to comprise a mecha-
O’Neal et al., 1994). have obvious functions for mitigating nism for sensing and coordinating re-
Studies of adaptive responses to specific types of stress, such as compati- sponses to the effects of thermal stress in
stress can be classified into two distinct ble solute transporters that facilitate the periplasm (Mecsas et al., 1993). Thus,
areas: the response itself and the ability transport of solutes in response to os- with F32 and FE, E. coli has separate and
to generate the response. Of particular motic stress (Loewen et al., 1998), while highly specialized systems for adapting to
interest in the response is how it miti- others may confer general protective thermal stress in the cytoplasmic and
gates the physiological consequences of properties under multiple stress condi- periplasmic compartments.
stress conditions. On the other side is tions.
the perception of stress, specifically how The GSR for one stress may induce Spore Formation
cells communicate the physical and changes that improve the organism’s sur-
chemical signals of ensuing stress condi- vival under other stress conditions, a phe- In addition to general and specific
tions to the regulatory machinery that nomenon known as cross protection. For stress response pathways, some bacteria
governs the response. Understanding the example, it has been demonstrated in lab- and other microorganisms also have
response mechanics will provide the in- oratory media that heat-shocking Salmo- evolved highly sophisticated pathways for
formation necessary to finely tune pro- nella Enteritidis (shifting the temperature stress adaptation, such as forming
cessing conditions to avoid triggering the from 20 C to 45 C) results in an approxi- spores. Spores are metabolically inactive
stress protection mechanisms. In addi- mate 3-fold increase in the D values (the or dormant and are much more resistant
tion, this knowledge can be used to de- time required to inactivate 90% of the or- to adverse environmental conditions,
velop rational targeting strategies to ganisms) at a pH of 2.6 and a greater than e.g., extremes of temperature, low water
identify novel antimicrobials for use in 10-fold increase when the temperature is activity, and radiation.
pre-harvest settings. raised to 56 C (Humphrey et al., 1993). In In organisms that form spores, the
this example, the original stress (exposure adaptive response pathways are somewhat
Responses to Stress to heat) increases protection to both heat hierarchical and, depending on the envi-
and acid even when the bacteria had not ronmental conditions, can be triggered
The cellular responses to stress can been previously exposed to low pH. alone or in combination. Bacillus subtilis,
generally be divided into two catego- the model organism for studying spore
ries—general and specific stress re- Specific Stress Response formation, relies on the general stress re-
sponses. In many instances, a certain sponse, several stationary phase and tran-
stress response gene may be part of One of the best-characterized exam- sition state pathways, the development of
both specific and general stress re- ples of specific stress response systems competence, and differentiation into the
sponse pathways. This is usually be- is the heat shock response. Like the GSR, dormant endospore. The pathways for
cause the gene has multiple regulatory the heat shock response involves an al- spore formation, competence, and normal
elements that are recognized by the dis- ternative sigma factor, F32, as a primary growth are mutually exclusive, but each
tinct machinery that coordinates the regulator. When the temperature in- one can be used in combination with the
general or specific response. It is there- creases, F32, which is normally degraded general stress response. Before the organ-
fore difficult to separate the contribu- rapidly, becomes more stable and is ism commits to a major step such as nor-
tion of general and specific stress re- translated at a higher rate, resulting in a mal growth, competence, or spore forma-
sponse pathways to cellular viability un- transient accumulation of the F32 pro- tion, sophisticated signal transduction
der any given stress condition. Rather, tein and a corresponding increase in the pathways measure environmental nutri-
the combination of the two, and specifi- rate of transcription from heat shock tional and chemical signals, as well as the
cally the combined fine-tuning of each promoters that are recognized by F32 state of cellular processes such as DNA
pathway, dictates many of the survival RNA polymerase (Morita et al., 2000). replication.
characteristics of the species. Approximately 30 proteins belong to the
heat shock regulon. Basal levels of the Role of Stress Adaptation
General Stress Response heat shock proteins are produced at all
temperatures, but at higher temperatures Scientific interest has recently focused
The general stress response (GSR) the microorganism needs a greater con- on determining the role of stress adapta-
regulon is a large group of genes that centration of these proteins to remain vi- tion pathways not only in the food matrix
collectively comprise several different able (Gross, 1996). Induction of the heat but also in a host or host cell. To some ex-
functions that facilitate growth and sur- shock response is somewhat more specif- tent, virulence genes can be considered an
vival under different conditions, such as ic than the GSR; however, there are other adaptive response to the stresses encoun-
osmotic shock, thermal stress, pH stress, triggers of the response, such as exposure tered during entry into the host. Studies
oxidative stress, and nutrient depletion to ethanol (Gross, 1996). Heat shock and have shown that components of specific
(Hengge-Aronis, 1996; Hengge-Aronis, the production of associated proteins and general stress responses are some-
2000; Lee et al., 1995). The GSR is a protects the cell from the detrimental ef- times necessary to survive entry into a

host cell. Specific examples include the
role of the general stress response regu-
latory protein rpoS in survival of Salmo- F38 Regulated Proteins 1993; Matin et al., 1989).
nella inside phagosomal vacuoles (Fang These protective proteins are likely
et al., 1992), the role of protease/chaper- Initially identified and character- involved in the ability of a pathogen to
one proteins in the intracellular survival ized in E. coli (Hengge-Aronis, 2000), survive the gastric acidity and other
of S. enterica and L. monocytogenes F38 homologues with analogous func- host defenses (Fang et al., 1992; Price
(Buchmeier and Heffron, 1990; Johnson tions have been identified in other en- et al., 2000). Moreover, F38 mediates
et al., 1991; Rouquette et al., 1996), and teric and nonenteric gram-negative expression of the SpvR virulence oper-
the role of acid tolerance genes in intrac- bacteria (Fujita et al., 1994; O’Neal et on in Salmonella (Robbe-Saule et al.,
ellular survival of L. monocytogenes al., 1994). The rpoS gene encoding for 1997) and the esp genes of pathogenic
(Marron et al., 1997). Because these F38 was initially identified as the mas- E. coli that encode for a Type III secre-
molecules facilitate survival in both the ter regulator of the phenotypic prop- tory system (Beltrametti et al., 1999)
food matrix and entry into a host cell, erties associated with stationary and consequently the virulence of
inducing these responses in the food ma- phase-reduced size and tolerance to these bacterial pathogens. Considering
trix could therefore “prime” the patho- a variety of physical and chemical the important functions of F38-regulat-
genic microorganisms, increasing their challenges (Hengge-Aronis, 1993; ed proteins, the finding of variations in
capacity to survive entry into a host cell Jenkins et al., 1988; 1990; Matin et al., the rpoS allele in stationary-phase cul-
and establish infection. 1989). The general stress tolerance in- tures of E. coli (Zambrano and Kolter,
Moreover, conditions in food pro- duced by stationary phase/starvation 1996) is of particular importance to
cessing environments that subject is primarily due to the effects of F38- the emergence of new strains of patho-
pathogens to sublethal stress may fur- regulated proteins, although the con- gens with enhanced survival or viru-
ther select pathogen subpopulations comitant morphological and physio- lence properties. These changes could
with increased survival efficiency (see logical changes likely contribute to result in enhanced production of these
sublethal injury, p. 63). Over time, these the stress-tolerance phenotype protective proteins and greater toler-
mechanisms could increase the relative (Hengge-Aronis, 1993; Kolter et al., ance to stress.
potential for a species to cause disease.
Using genome-based methodologies in Table 4. Functions of F-Regulated Proteins
food processing research centers, future
scientists will be able to examine the Function Example Reference
populations of species that survive food Metabolic changes otsBA operon, trehalose metabolism Hengge-Aronis, 2000
processing conditions.
Protection Oxidative stress protection by dps Altuvia et al., 1994

Signal Perception and Induction Oxidative stress protection by katE, Mulvey et al., 1990
catalase HPII
In addition to different stress re-
sponses, microorganisms have evolved Repair aidB, repairs methylation damage Landini et al., 1996
multiple and unique mechanisms (path- of DNA
ways) for sensing and transducing physi-
cal and chemical signals to the regulatory
machinery that coordinates stress re-
sponses. It should be noted, however, polymerase subunit. F38 accumulates dur- primarily by its accessibility, not by its
that distinguishing between the impact ing several different stress conditions and rate of synthesis or degradation. When
of the regulatory machinery and slight activates the target genes that produce the under stress, the organism produces an-
variations in the actual responses is diffi- general stress response. The rate of syn- other protein (the anti-sigma factor) that
cult. Examining the mechanics of signal thesis for the RpoS protein increases little binds with the FB protein, making it no
perception and transduction can yield during stress conditions; it accumulates longer accessible (Benson and Halden-
new insights into optimizing the safety of rapidly after stress because the degrada- wang, 1993). The anti-sigma factor pro-
food production processes and can pro- tion rate is slowed. Unlike most response tein is controlled by a complex cascade of
vide specific targets for design of antimi- regulators, which directly modulate gene signal transduction proteins, which ap-
crobial agents. transcription by increasing the amount of pears to form branched pathways of sig-
Detailed analyses of distantly related signal protein produced, this response nal flow and provides several points of
bacteria reveal that similar stress re- regulator functions by controlling the sta- entry for different types of signals. Be-
sponses may be modulated by very dif- bility of the protein and thereby changing cause many of these signal transduction
ferent regulatory machinery. For exam- its rate of degradation. proteins appear to bind to ribosomes, sci-
ple, gram-negative enteric bacteria and In the instance of the GSR of gram- entists have hypothesized that stress in the
low G+C gram-positive organisms use positive bacteria, much is known about cytoplasm is measured by increases in ri-
different mechanisms to trigger similar B. subtilis. As in the gram-negative bac- bosome dysfunction.
stress responses. teria, the GSR in B. subtilis is modulated Despite differences in regulatory ma-
In gram-negative bacteria, the GSR primarily by an alternative sigma sub- chinery, there is striking similarity be-
pathway is modulated primarily by a pro- unit of RNA polymerase, in this case tween the stress protection system(s) of
tein called F38 or RpoS, which is an RNA known as FB. However, FB is controlled distantly related bacteria such as E. coli


and B. subtilis. Several genes in the RpoS- (Becker et al., 1998). Given that this al foodborne pathogens. Understanding
mediated stress protection system in E. gene, known as rsbX, is the first regula- them may enable scientists to predict
coli have homologues in B. subtilis that tor in the signal transduction pathway, future foodborne pathogens with great-
are part of the F32 stress protection sys- the divergence could be intimately as- er accuracy.
tem regulon. The shared genes of the re- sociated with the specialized physiolo-
spective stress protection systems likely gy of the two species. A second exam- Driving Forces in Pathogenicity
constitute a core collection of important ple of the divergence is observed in S.
functions that confer the general protec- aureus, which lacks three of the seven Primary drivers of microbial
tive properties needed for exploiting soil collinear regulatory genes (Kulick and pathogenicity are the growth in the hu-
and intestinal environments. Giachino, 1997; Wu et al., 1996). Al- man population and the proportion of
Despite the similarity of the E. coli though the precise meaning of these the population that is immunocom-
and B. subtilis stress protection system examples of divergence in regulatory promised either because of age, preg-
regulons, there are also some clear differ- molecules is not known, one might nancy, underlying disease, or immuno-
ences. For example, several heat shock generally conclude that the differences suppresive treatments. With higher
genes in the B. subtilis stress protection reflect fine-tuning of the regulatory densities of humans, microbes can ex-
system are governed independently of machinery to the physiological needs ploit a multitude of routes to transfer
the stress protection system in E. coli of the species. from an infected person to other hu-
where they are modulated primarily by The function of the regulatory ma- mans. The concentration of humans in
the heat shock regulons. chinery also is likely to be fine-tuned in urban settings can select for microbes
Comparing the FB-mediated stress both signal perception and the target that are transmitted from person-to-
protection system in the closely-related genes of the regulons. Studies with B. sub- person or through contaminated air,
species B. subtilis, L. monocytogenes, tilis and L. monocytogenes have shown that food, and water. The same case can be
and S. aureus, reveals clear instances of the magnitude of the stress protection sys- made for high-density farms raising
divergent evolution despite the similar- tems to different types of signals is spe- meat animals or food crops. World-
ity of the regulatory machinery. In B. cies-specific. For example, osmotic shock wide human travel and the global dis-
subtilis and L. monocytogenes, the seven triggers a relatively minor response in B. tribution of foods facilitate the intro-
regulatory genes that modulate FB ac- subtilis but in L. monocytogenes is one of duction and flow of pathogens and ex-
tivity are collinear and comprise an the most potent inducers (Becker et al., otic microbial genes into human and
operon including the FB gene itself. 1998). Consequently, the stress protec- animal populations.
Despite the collinearity in position, tion system contributes little to the growth In the absence of a properly func-
there is not a corresponding collineari- of B. subtilis in conditions of high osmo- tioning immune system, microbes that
ty in structure; the distal gene of the larity, but for growth of L. monocytogenes are harmless to a majority of the popu-
operon shares only distant similarity the contribution is significant. lation can cause life-threatening infec-
with its homologue in the other species Collectively, stress protection sys- tions in immunocompromised individ-
although the upstream genes are gener- tems play pivotal roles in the survival, uals. People older than 65 years of age
ally much more similar to one another dissemination, and virulence of bacteri- generally have reduced immunity that

Emergence of Viruses,
agents as compared to the emerging impact of environmental pollution as
Parasitic Protozoa and bacterial agents such as L. monocytoge- a contamination source.
nes or E. coli O157:H7. Finally, the The prevalence of viral gastroen-
Marine Biotoxins as ability to work with many of these teritis in the United States and world-
agents has been restricted by method- wide has been drastically underesti-
Foodborne Pathogens ological limitations that have been par- mated for many years. For instance,
Although pathogenicity of some tially overcome by the introduction of public health officials have consis-
of the marine biotoxins has been routine molecular biological tech- tently failed to report and investigate
characterized, there is a paucity of niques. outbreaks of mild gastrointestinal
information available regarding the New knowledge has emerged that disease, in part because of a lack of
disease mechanisms or virulence highlights the unique nature of these resources. In the absence of reliable
factors for enteric viruses and para- agents. This information has been ob- laboratory methods, there has been a
sitic protozoa. The reasons for this tained largely through: (1) increased general reluctance on the part of pub-
are several-fold; for many of these epidemiological surveillance; (2) im- lic health officials to classify food-
agents, in vitro cultivation and/or proved detection methods; and (3) in- borne outbreaks as viral solely on the
animal models are nonexistent. Be- creased research funding in food safety. basis of epidemiological criteria
cause they have had relatively less Such initiatives have helped scientists (Bean et al., 1990). Today, clinical
scientific emphasis over the last few understand infectious doses, the role labs are using molecular biology
decades, fewer research dollars have of ever-increasing internationalization techniques such as the polymerase
gone into understanding these of the food supply and the increased Continued on next page

continues to decline with age. By 2050,
the U.S. human population will reach
Continued from previous page an estimated 400 million, and, of this
population, 80 million will be 65 years
chain reaction to facilitate diagno- handler hygiene, which is likely to of age or older. This growth in immu-
sis of infected patients, although be less advanced in developing na- nocompromised populations will cer-
these methods are not yet adapted tions and hence may contribute di- tainly affect the number of cases of
to the routine detection of viruses rectly or indirectly to the safety of foodborne illness associated with op-
in contaminated foods. These foods imported into the United portunistic pathogens, which will be-
same methods are being used to States. As with the viruses, human come much more prevalent.
identify genetic relatedness be- challenge studies are currently un- In terms of the environment, mi-
tween human caliciviruses and derway in an effort to better under- crobes continue to evolve to gain a
similar viruses detected in stool stand the infectious doses of the competitive advantage, and, as advanc-
samples obtained from farm ani- parasitic protozoal pathogens. Al- es are made to eliminate or control one
mals, sparking the debate that ani- though detection methods exist and pathogen, another organism will
mals may be a reservoir for the refinements are being reported, the quickly occupy the niche that has been
NLVs and concern over the poten- routine implementation of these vacated, known as “niche filling”. In
tial for zoonotic transmission (van screening methods requires highly some cases, the new organism that oc-
der Poel et al., 2000). Other inves- trained personnel, and scientists are cupies this niche may be more patho-
tigators have focused their efforts unable to detect parasitic protozoa genic than the original pathogen or
on tracking epidemics in both in contaminated foods at the may employ a different mechanism of
space and time, concluding a win- present time. virulence that is more detrimental to
ter-spring seasonality of NLV out- With respect to the marine human hosts (see shifts known patho-
breaks; the presence of many ge- biotoxins, much has yet to be gens, p. 22).
netically different variants, sug- learned. While the mechanisms of In addition, microbiological ecolo-
gesting that most outbreaks are in- pathogenesis of some of the known gy involves the interplay of climate
dependent events; and on occa- biotoxins has been elucidated, the changes, pollution, and genetic ex-
sion, the presence of a common, emerging agents such as Pfiesteria change that selects for and perhaps
predominant strain, without obvi- have not been characterized. In fact, drives the generation of new microbial
ous epidemiological link, that the purified toxins cannot always be strains. Changes within an ecosystem
emerges, spreads and then disap- isolated. In many instances, scien- whereby the micro- and macro-popu-
pears (Fankhauser et al., 1998). tists do not fully understand the lations of organisms are out of bal-
There are also ongoing research stimulation required for the pro- ance, selecting for new variants with a
initiatives to ascertain the infec- duction of HABs. While many competitive advantage, is one theory
tious dose of representative NLVs HABs may be associated with nor- that has been proposed to explain the
such as the Norwalk agent and the mal fluctuations in nutrient input emergence of new variants of existing
Snow Mountain agent. Taken to- and water temperature in the estua- microbes.
gether, these factors will continue rine environment, it is likely that In terms of increased virulence in
to contribute to the emergence of nutrient loading associated with or- pathogens, two themes should be em-
this important group of foodborne ganic and inorganic pollution may phasized. First, many of the stress re-
pathogens. contribute to their increased preva- sponse systems that contribute to sur-
We also do not yet understand lence and perhaps to the emergence vival in the food matrix also contribute
the importance of foods as vectors of new toxic algal species. In the to survival during passage through the
for parasitic protozoan disease, al- southeastern United States, some gastrointestinal tract and the invasion
though it is likely that this will be have cited intensive animal agricul- of host cells. If this phenomenon
better defined in the coming de- ture practices and/or increased land proves to be a significant feature of
cades. Unlike the viruses which development with associated popu- “virulence” for a species, then pre-har-
are only transmitted by humans, lation density increases as providing vest environments and food processing
animal fecal pollution, and associ- the necessary environmental forces. conditions should be designed to avoid
ated runoff from farms may con- Certainly, ongoing epidemiological imposing sublethal stress and hence
tribute substantially to the con- studies will help ascertain the true selection of resistant bacterial popula-
tamination of water and subse- public health impacts of these new tions. Secondly, the diversity of stress
quently crops. International trade toxic algae. In all instances (viruses, regulatory response systems and regu-
issues have certainly impacted the parasitic protozoa, and marine latory molecules holds promise for ra-
emergence of C. cayetanensis, but biotoxins), continued emphasis on tional design and targeting of antimi-
the importance of poor water research and vigilant surveillance crobial agents that eliminate pathogen
quality as opposed to direct con- will likely result in reports of in- populations while minimizing the dis-
tamination by local wildlife has creased prevalence, and hence ruption of the total bacterial popula-
not yet been determined. This “emergence,” of these agents as as- tion. Such agents could be used in pre-
does, however, bring up the critical sociated with human foodborne and post-harvest settings, such as feeds
issue of water quality and food disease. and carcass washes to facilitate elimi-
nation of unwanted species.


Pathogenicity of Brees et al., 2000). As many as half of all target certain cells, including the en-
E. coli O157:H7 cattle carry O157:H7 at some time in dothelial cells of blood vessels; the
their lives, and some observers suggest dead cells accumulate and plug the
E. coli O157:H7 is typical of what that nearly all cattle have been exposed kidney, causing HUS. Shiga toxin is
might be expected in terms of an to EHEC. The organisms are introduced encoded within a mobile genetic ele-
emerging pathogen. into the environment through the feces, ment, a bacteriophage, that enables it
including manure used as fertilizer for to move to different strains of bacteria.
Nomenclature food crops. Rainwater runoff can then As discussed below, it is believed that
spread them to water reservoirs and the acquisition of this toxin by E. coli is
E. coli O157:H7 belongs to a wells. Alternately, fecal contamination at a relatively recent genetic event.
group of E. coli (enterohemhorrhagic slaughter may result in meat contamina- In addition to producing Shiga
E. coli, EHEC) that cause hemorrhag- tion. In addition to cattle, other rumi- toxin, EHEC adhere to the large bowel,
ic colitis (severe bloody diarrhea) and, nants, such as goats and sheep, and wild the pathogen’s preferred site in the
in a small portion of the cases, ruminants, such as deer, can carry this body, using a variety of virulence fac-
hemolytic uremic syndrome (HUS). organism, and it has now been found in tors contained within the LEE patho-
These strains are within a larger birds, flies, and in the food-producing genicity island. This 38-kb region of
group of Shiga-toxin-producing E. environment. DNA, inserted near a tRNA gene, con-
coli (STEC), but EHEC possess viru- Tolerance to low pH facilitates pas- tains all the genes necessary for bind-
lence factors that other STEC do not. sage through the stomach, making it pos- ing to epithelial cells and causing a
EHEC have been the source of many sible for E. coli O157:H7 to cause disease pedestal to form on their surface. Ped-
food- and water-borne outbreaks. It at a low infectious dose (10-100 bacte- estals are created when actin in the cy-
has been estimated that these patho- ria). The organism’s acid tolerance also toplasm is accumulated and polymer-
gens cause about 75,000 cases of diar- allows it to survive within acidic food, ized beneath the pathogen. In addi-
rhea and several hundred deaths an- which was a major factor in outbreaks of tion, effacement of the microvilli oc-
nually in the United States (Mead et illness traced to unpasteurized apple curs, giving rise to the term “attaching
al., 1999). Young children and older juice, a product with a pH of approxi- and effacing E. coli”. Pedestal forma-
adults are particularly susceptible to mately 3.5 that usually inhibits the less tion is a complex process that utilizes a
HUS, while people of all ages can get virulent strains of E. coli. Type III secretion system, several Type
the diarrhea. In the past few years, scientists have III E. coli secreted proteins (Esp’s), and
The designation O157:H7 is based made significant advances in under- a key molecule, Tir (Translocated in-
on serological analysis: lipopolysac- standing the underlying virulence mech- timin receptor), that is delivered to
charide (O) type 157, and flagellar (H) anisms of EHEC strains. Two major vir- host cell membranes. Once in the host
type 7. However, scientists have since ulence pathways contributing to disease cell membrane, Tir binds to intimin, a
discovered that several related E. coli have been identified, although there are bacterial outer membrane protein, re-
strains with different O serotypes probably many others yet to be discov- sulting in intimate bacterial adherence.
cause similar disease, such as ered. To cause disease, EHEC must pos- Because Tir spans the host membrane,
O26:H11. Although O157:H7 is the sess a Shiga toxin gene and genes within it is also able to recruit host cytoskele-
most predominant EHEC serotype in the LEE pathogenicity island that enable tal proteins to cause actin accumula-
North America, Japan and the United the bacteria to adhere to epithelial cells tion and pedestal formation.
Kingdom, different serotypes of EHEC and form a pedestal on the epithelial sur-
such as O26:H11 and O111:NM dom- face upon which the bacteria reside. The Emergence
inate in other areas of the world, nota- attaching and effacing genes also are
bly central Europe and Australia. Be- found in enteropathogenic E. coli E. coli O157:H7 is believed to have
cause of the conservation of virulence (EPEC), a common cause of watery diar- arisen from a series of fairly recent ge-
factors, but not serotypes, classifica- rhea in the developing world, but these E. netic events. O157:H7 was first report-
tion schemes of EHEC strains should coli lack the Shiga toxin gene and, possi- ed as a foodborne pathogen following
probably be based on virulence factors bly, other virulence factors present in an outbreak associated with contami-
rather than the variant serotype. How- EHEC. nated hamburgers in 1982. Subse-
ever, O157:H7 (EHEC 1) and The Shiga toxins are comprised of quent studies of diarrheal samples
O26:H11/O111:NM (EHEC 2) clearly two components, A and B subunits, that from prior outbreaks and sporadic
comprise two distinct genetic lineages. structurally resemble other toxins such cases revealed only a single E. coli
as cholera toxin. The B subunit confers O157:H7 isolate in the Center for Dis-
Virulence tissue specificity, enabling the toxin to ease Control and Prevention’s collec-
adhere to a specific glycolipid receptor, tion. This isolate had been obtained
E. coli O157:H7 and related globotriaosylceramide (Gb3), on cell from an individual in the mid-1970s.
strains have the capacity to persist in surfaces. The active (A) portion of the A closely related strain of E. coli called
cattle without causing disease because toxin is then delivered into the host cell enteropathogenic E. coli (EPEC) causes
cattle lack a receptor for the illness- where it inhibits protein synthesis, ulti- diarrhea in children (but does not
producing Shiga toxin (Pruimboom- mately killing the host cell. The toxins Continued on next page

Continued from previous page in expression. Kimmitt et al. (2000) re- pies use an inert substance that mim-
cause HUS). EPEC contains the ported that some antimicrobial agents, ics the toxin’s glycolipid receptor. In-
LEE locus, but not the Shiga toxin. particularly quinolones, trimethoprim, gestion of the mimicking substance
It is believed that EHEC arose when and furazolidone, were shown to induce should bind excess toxin and thereby
an EPEC-like organism (containing toxin gene expression and should be limit disease progression. Experi-
the LEE island) acquired a Shiga avoided in treating patients with poten- ments indicate it may be effective, but
toxin via a bacteriophage. This tial or confirmed STEC infections. These only when taken very early after in-
event has occurred on more than investigators also reported, however, that fection. Alternate therapies are being
one occasion, leading to the two dis- results of available studies conflict with explored.
tinct EHEC lineages. Experimental regard to the influence of antibiotics, In addition, significant effort is
evidence comes from studies done in noting that age group, timing of antibiot- focused on developing treatments
rabbits, where a LEE-encoding E. ic therapy, and range of agents used such as vaccines and probiotics to
coli was altered to also encode the complicate the analyses. Further, Kim- reduce carriage of O157:H7 by cat-
Shiga toxin. The resulting pathogen mett et al. (2000) reported that their ob- tle. Decreasing the level of O157:H7
produced a diarrhea that resembled servations suggest that the complex in- in cattle would significantly decrease
hemorrhagic colitis, which was an terplay of infection stage, number of or- the potential for food and water
EHEC-like disease. ganisms present at the time antibiotics contamination. Similarly, childhood
are administered, and the environmental vaccines are being developed, but
Treatment conditions of those microorganisms, given the low incidence of disease,
coupled with time-concentration profile, questions remain about whether
Therapies against EHEC infec- and bactericidal effect of the drug, could universal vaccination should be em-
tions are extremely limited. Treat- render an antibiotic clinically beneficial, ployed, were an effective vaccine to
ment with antibiotics is thought to neutral, or disadvantageous in different be developed. Experimental ap-
worsen the illness, presumably by situations. proaches to block virulence factors
breaking up the bacteria, which re- One potential therapeutic is current- such as the Type III secretion system
leases more toxin and increases tox- ly in phase III clinical trials. New thera- also are being studied.

Humans as Hosts of Foodborne Disease

A number of factors that relate to the exposure. For example, assuring quired by consumption of food contain-
human host have a major impact on the proper handling and cooking of ing pathogens or their toxins. The patho-
gens or their toxins can damage or de-
occurrence and severity of foodborne ground beef contaminated with stroy host cells or processes, or they can
disease. The host’s age, gender, place of Escherichia coli O157:H7 could induce a host response to their presence
residence, ethnicity, educational that is harmful to the human host. Food-
eliminate that food safety risk even in
borne illness is caused by: viral, bacterial,
background, underlying health status, the presence of continuing contamina- or parasitic infections (e.g., Norwalk-like
and knowledge, attitudes, and practices tion of raw ground beef. Obviously, viral gastroenteritis, Campylobacter en-
related to health and diet all have teritis, toxoplasmosis); toxins produced
risk communication is an essential tool
during microbial growth in food (e.g.,
important bearing on foodborne for preventing foodborne illness. Clostridium botulinum, Staphylococcus
illness. The health of the host affects However, successful control requires aureus, Bacillus cereus, and Aspergillus
the individual’s susceptibility to flavus); and toxins produced by algal and
effective interventions at all stages of fungal species (e.g., ciguatera fish poi-
infection and illness, and the host’s
the food system. soning) (see Table 5).
dietary and hygiene practices affect Foodborne infections occur when
exposure to pathogens. From medical Manifestations of Clinical Disease pathogenic microorganisms are ingested,
colonize the intestine, and sometimes in-
and behavioral perspectives, human
As the name implies, foodborne dis- vade the mucosa or other tissues. Food-
host factors can be altered by modifica- eases—including intoxication, infection, borne toxicoinfections arise when a mi-
tion of susceptibility or elimination of and toxicoinfection—are illnesses ac- croorganism from ingested food grows


Continued from previous page in expression. Kimmitt et al. (2000) re- pies use an inert substance that mim-
cause HUS). EPEC contains the ported that some antimicrobial agents, ics the toxin’s glycolipid receptor. In-
LEE locus, but not the Shiga toxin. particularly quinolones, trimethoprim, gestion of the mimicking substance
It is believed that EHEC arose when and furazolidone, were shown to induce should bind excess toxin and thereby
an EPEC-like organism (containing toxin gene expression and should be limit disease progression. Experi-
the LEE island) acquired a Shiga avoided in treating patients with poten- ments indicate it may be effective, but
toxin via a bacteriophage. This tial or confirmed STEC infections. These only when taken very early after in-
event has occurred on more than investigators also reported, however, that fection. Alternate therapies are being
one occasion, leading to the two dis- results of available studies conflict with explored.
tinct EHEC lineages. Experimental regard to the influence of antibiotics, In addition, significant effort is
evidence comes from studies done in noting that age group, timing of antibiot- focused on developing treatments
rabbits, where a LEE-encoding E. ic therapy, and range of agents used such as vaccines and probiotics to
coli was altered to also encode the complicate the analyses. Further, Kim- reduce carriage of O157:H7 by cat-
Shiga toxin. The resulting pathogen mett et al. (2000) reported that their ob- tle. Decreasing the level of O157:H7
produced a diarrhea that resembled servations suggest that the complex in- in cattle would significantly decrease
hemorrhagic colitis, which was an terplay of infection stage, number of or- the potential for food and water
EHEC-like disease. ganisms present at the time antibiotics contamination. Similarly, childhood
are administered, and the environmental vaccines are being developed, but
Treatment conditions of those microorganisms, given the low incidence of disease,
coupled with time-concentration profile, questions remain about whether
Therapies against EHEC infec- and bactericidal effect of the drug, could universal vaccination should be em-
tions are extremely limited. Treat- render an antibiotic clinically beneficial, ployed, were an effective vaccine to
ment with antibiotics is thought to neutral, or disadvantageous in different be developed. Experimental ap-
worsen the illness, presumably by situations. proaches to block virulence factors
breaking up the bacteria, which re- One potential therapeutic is current- such as the Type III secretion system
leases more toxin and increases tox- ly in phase III clinical trials. New thera- also are being studied.

Humans as Hosts of Foodborne Disease

A number of factors that relate to the exposure. For example, assuring quired by consumption of food contain-
human host have a major impact on the proper handling and cooking of ing pathogens or their toxins. The patho-
gens or their toxins can damage or de-
occurrence and severity of foodborne ground beef contaminated with stroy host cells or processes, or they can
disease. The host’s age, gender, place of Escherichia coli O157:H7 could induce a host response to their presence
residence, ethnicity, educational that is harmful to the human host. Food-
eliminate that food safety risk even in
borne illness is caused by: viral, bacterial,
background, underlying health status, the presence of continuing contamina- or parasitic infections (e.g., Norwalk-like
and knowledge, attitudes, and practices tion of raw ground beef. Obviously, viral gastroenteritis, Campylobacter en-
related to health and diet all have teritis, toxoplasmosis); toxins produced
risk communication is an essential tool
during microbial growth in food (e.g.,
important bearing on foodborne for preventing foodborne illness. Clostridium botulinum, Staphylococcus
illness. The health of the host affects However, successful control requires aureus, Bacillus cereus, and Aspergillus
the individual’s susceptibility to flavus); and toxins produced by algal and
effective interventions at all stages of fungal species (e.g., ciguatera fish poi-
infection and illness, and the host’s
the food system. soning) (see Table 5).
dietary and hygiene practices affect Foodborne infections occur when
exposure to pathogens. From medical Manifestations of Clinical Disease pathogenic microorganisms are ingested,
colonize the intestine, and sometimes in-
and behavioral perspectives, human
As the name implies, foodborne dis- vade the mucosa or other tissues. Food-
host factors can be altered by modifica- eases—including intoxication, infection, borne toxicoinfections arise when a mi-
tion of susceptibility or elimination of and toxicoinfection—are illnesses ac- croorganism from ingested food grows


Table 5. Causes of Foodborne Illness pathogens. E. coli O157:H7 is most com-
monly associated with undercooked
Type of Causative Agent ground beef and causes severe cramping
Example(s) Frequency (in the U.S.)
and bloody diarrhea. After the hemor-
Bacterial infection Campylobacter jejuni Common rhagic colitis caused by E. coli O157:H7
Viral infection
and other enterohemorrhagic E. coli
Norwalk-like viruses Very common
(EHECs), some children develop a char-
Parasitic infection Toxoplasma gondii Relatively common acteristic set of kidney disfunction and
anemia called hemolytic uremic syn-
Bacterial toxin Clostridium perfringens, Relatively common
drome (HUS). In the United States, HUS
Bacillus cereus is the leading cause of acute kidney fail-
Algal toxin Ciguatera fish poisoning Less common ure in children.
The major effects of some foodborne
Mycotoxin Aflatoxin Less common pathogens are outside the gastrointesti-
Prions* BSE None nal tract. Listeria monocytogenes causes
serious illness in pregnant women, their
Inorganic contaminants* Heavy metals Less common fetuses, or newborns, often resulting in
Organic contaminants* Pesticide residues Less common spontaneous abortion or stillborn ba-
bies. An estimated 92% of foodborne
cases of listeriosis result in hospitaliza-
* Not addressed within this report.
tion, and 20% result in death. C. botuli-
num produces toxins that attack the cen-
in the intestinal tract and elaborates a (Mead et al., 1999), result in nausea, tral nervous system, resulting in weak-
toxin(s) that damages tissues or inter- vomiting, headache, diarrhea, and ab- ness, vertigo, double vision and difficulty
feres with normal tissue/organ function. dominal pain. The symptoms usually swallowing and speaking.
Foodborne microbial intoxications oc- subside within a day or two, and the in- In addition to acute illness, some
cur by ingestion of a food containing fections rarely come to the attention of foodborne pathogens cause chronic ill-
harmful toxins or chemicals produced by public health workers. ness, often within sensitive subgroups of
the microorganisms, usually during their However, some pathogens cause gas- the population. For example, hepatitis A
growth in the food. trointestinal symptoms that are more se- virus (HAV) causes fever, headache, an-
Despite our best efforts, foodborne vere and take longer to subside, especial- orexia, malaise, nausea, abdominal dis-
diseases remain common. Based on the ly in immunocompromised individuals comfort and sometimes jaundice. These
available data, the Centers for Disease such as young children, the elderly or symptoms usually take weeks to resolve.
Control and Prevention (CDC) has esti- people with AIDS. For example, Within a genetically predisposed sub-
mated that 76 million cases of foodborne Cryptosporidium parvum is a parasitic group, prolonged HAV infection may be
illness occur annually resulting in protozoan that causes severe watery diar- the precipitating event in the onset of au-
325,000 hospitalizations and 5,000 rhea and sometimes coughing, fever, and toimmune chronic active hepatitis
deaths (Mead et al., 1999). intestinal distress. Symptoms may last (Bogdanos et al., 2000; Naniche and Old-
Most infectious foodborne illness is from four days to three weeks. Campylo- stone, 2000; Rahyaman et al., 1994.
characterized by acute symptoms that are bacter jejuni, usually associated with raw The foodborne parasite Toxoplasma
limited to the gastrointestinal tract, in- chicken and raw milk, can trigger watery gondii causes birth defects. In addition,
cluding vomiting and diarrhea. These ill- diarrhea, fever, abdominal pain, and chronic toxoplasmic encephalitis attrib-
nesses are generally limited in both dura- nausea that last for days to weeks. Of the uted to T. gondii infection may occur
tion and severity, and most patients estimated illnesses attributed to known when an individual’s immune system is
without underlying illnesses or malnu- foodborne pathogens, Campylobacter impaired. Toxoplasmal encephalitis,
trition recover without medical treat- spp. are responsible for more than 14% characterized by dementia and seizures,
ment or require only modest supportive (Mead et al., 1999). has become the most commonly recog-
care. These illnesses can be especially dif- Not all foodborne disease is limited nized cause of opportunistic infection of
ficult to quantify because medical treat- to the gastrointestinal tract. Some food- the central nervous system in AIDS pa-
ment is not sought. For example, B. borne pathogens invade deeper tissues or tients. Activated macrophages, lympho-
cereus—linked to a wide variety of foods produce toxins that are absorbed and cytes, and cytokines play a major role in
such as meat, milk, vegetables, fish, and cause systemic symptoms, including fe- control of both the acute infection and
rice products—may cause diarrhea and ver, headache, kidney failure, anemia, maintenance and/or prevention of the
abdominal cramps and pain that last ap- and death. Salmonella has been linked to chronic stage (Cohen, 1999; Tenter et al.,
proximately one day. C. perfringens, numerous foods, but especially raw 2000).
which may be present in meat, meat meats, poultry, and eggs. The symptoms Biotoxins also cause foodborne dis-
products and gravies, can cause intense of salmonellosis include nausea, vomit- ease, with both acute and chronic clinical
abdominal cramps and diarrhea that ing, abdominal cramps, fever, and head- manifestations. Because these com-
also generally resolve within a one-day aches with a duration that ranges from pounds can be resistant to processing
period. Norwalk-like viruses, responsible days to weeks. Nontyphoidal Salmonella and cooking, biotoxins can be present in
for an estimated 66.6% of illnesses at- are responsible for an estimated 30.6% a food even in the absence of viable cells
tributed to known foodborne pathogens of deaths caused by known foodborne of the causative agent. The target organs

for these toxins vary and can include the dence indicates GBS is an autoimmune the urogenital system. A genetic predis-
liver, kidney and gastrointestinal tract as disease, but the immunologic mecha- position to developing post-infectious
well as the immune, nervous, and repro- nisms that produce GBS after infection reactive arthritis has been documented in
ductive systems. Biotoxins include toxins with C. jejuni are complex. Studies sup- persons who share certain genetic traits.
produced by bacteria (e.g., botulism tox- port the hypothesis of molecular mimic- Other genes acting in concert apparently
in), fungi (e.g., aflatoxin and fumonisin), ry, since peripheral nerves may share determine the clinical presentation.
marine organisms such as dinoflagellates epitopes with surface antigens of certain Chronic sequelae are thus related to ge-
(ciguatoxin), and plants (phytotoxins, strains of C. jejuni. Some data suggest netically determined host risk factors in
which are not discussed in this report). that patients share genetic traits (Smith, combination with an environmental trig-
The chronic sequelae of foodborne 1995). Although it is clear that GBS is an ger (Kobayashi and Ando, 2000; Parker
infections in particular often focus on autoimmune phenomenon, evidence in- and Thomas, 2000). It is important to
extra-intestinal systems, although food- dicates that infections with C. jejuni, a note that as human and microbial ge-
borne microorganisms also may play a common foodborne pathogen, frequent- nome sequencing projects progress, sci-
role in chronic enteropathies such as in- ly start the pathologic process (Allos, entists should gain increasing insights
flammatory bowel disease. Guillain-Bar- 1997; Shoenfeld et al., 1996). into the bacterial virulence factors and
ré Syndrome (GBS) is a disorder of the Another example of chronic illness the host factors that interact in the pro-
peripheral nervous system that occurs related to a foodborne infection is reac- duction of these chronic, autoimmune
worldwide and is a common cause of tive arthritis. Triggered by infection with pathologies. Hopefully, these insights
neuromuscular paralysis. Victims lose Yersinia enterocolitica, Yersinia pseudotu- will eventually result in rational thera-
the ability to write or speak and experi- berculosis, Shigella flexneri, Shigella dys- pies to prevent or treat these types of dis-
ence motor paralysis with mild sensory enteriae, Salmonella spp., C. jejuni, and E. eases.
disturbances. Cases of severe GBS have coli, reactive arthritis is an acute sterile Although the evidence is not com-
been linked to a previous infection with inflammation of the joints. In addition plete, foodborne infections may play a
C. jejuni, although other enteric patho- to joint pain, Reiter’s syndrome, a sub- role in the development of inflammatory
gens also may trigger the disorder. Evi- type of reactive arthritis, affects eyes and bowel disease (IBD). IBD is the collective

Pfiesteria piscicida
and Pfiesteria-like cally related organisms (MROs). MROs lipophilic components, which may be
are believed to occur in waters from responsible for fish morbidity and
Microbes As Potential Delaware to the Gulf of Mexico (EPA, mortality (Fleming et al., 1999; Noga,
1998). Currently, the number of MROs 1997). Reported human impacts in-
Foodborne Pathogens is unknown, and while some are toxic, clude respiratory irritation, skin rash-
An association between seafood- others are not (Steidinger and Penta, es and possible neurocognitive disor-
borne illness in humans and the oc- 1999). ders (Glasgow et al., 1995). Although
currence of Pfiesteria in the marine It has been proposed that the Pfieste- animal models have been developed
environment has not been estab- ria dinoflagellate, unlike most toxic di- to investigate neurocognitive effects
lished, and much remains unknown. noflagellates, excretes its toxin(s) into the (Levin et al., 1997), and epidemiologi-
Pfiesteria piscicida and Pfiesteria-like estuary rather than retaining the toxin cal studies to evaluate the potential
organisms, discovered in 1988, have within its cell (Burkholder et al., 1995; human health effects (Gratten et al.,
caught the attention of researchers Glasgow et al., 1995). Following expo- 1998; Savitz, 1998) are ongoing, re-
and funding agencies interested in sure to toxic P. piscicida and other toxic sults are inconclusive to date.
characterizing the biological func- MROs, fish appear to be narcotized and It is important to note that all of
tions and effects of previously unrec- frequently die (Burkholder et al., 1995; these studies investigate transmission
ognized toxic dinoflagellates (Flem- Glasgow et al., 1995; Noga, 2000). How- routes other than through the con-
ing et al., 1999; Glasgow et al., 1995; ever, the toxin (Pptx) is relatively unsta- sumption of contaminated seafood.
Smith et al., 1988). Initially present- ble in the marine system, and in spite of Nonetheless, consumer confidence in
ing as the cause of massive fish kills continuing research efforts on the life cy- seafood is adversely affected by
in North Carolina in the late 1980s, cle and physiology of Pfiesteria, very little events such as fish kills and health
Pfiesteria-like organisms also have is known about the toxin(s) produced by alerts. Extensive media coverage of
stimulated public concern over the the dinoflagellate. Attempts to obtain Pfiesteria, closings of recreational
potential threat these organisms may purified toxin(s) have been unsuccessful. and commercial waters, as well as a
have on human health and seafood Mechanisms of action and chemical growing list of scientific unknowns
safety. Because of difficulties in iden- structure are currently undetermined. regarding the organism’s occurrence,
tification of the Pfiesteria species, Investigators believe that the toxin con- toxin(s), and effects, have generated
these organisms are currently charac- sists of both water-soluble fractions, immediate food safety concerns in
terized on the basis of morphology which may be responsible for the alleged seafood consumers, despite the ap-
and hence referred to as morphologi- neurotoxic effects in humans, and highly parent safety of these foods.


term for Crohn’s disease (CD) and ul- duced. Many factors cause these systems tration by microbes and their toxins.
cerative colitis (UC), which are both to function below optimal levels, increas- Fortunately, the body defends itself
chronic inflammatory diseases with a ing the likelihood of illness. In addition, with an extraordinary array of non-
prolonged clinical course. Abdominal some foodborne pathogens have found specific and specific immune mecha-
abscesses are a complication of CD ways to evade or trick the body’s defen- nisms.
while in UC abdominal perforations sive mechanisms.
may lead to peritonitis. The cause of Nonspecific Immune Mechanisms
IBD, and the mechanism(s) for sponta- Immune Response
neous exacerbations and remissions re- Nonspecific or “innate” immunity is
main unresolved. Controversial reports Foodborne pathogens and their the front line of host defense against mi-
by some investigators about the poten- toxins enter human tissue via the gas- croorganisms in the gut and other sites
tial association of Mycobacterium trointestinal (GI) tract. The GI tract is (Elwood and Garden, 1999; Pestka,
paratuberculosis, the etiologic agent of approximately 30 feet long and in- 1993; Takahashi and Kiyono, 1999). The
Johne’s disease in ruminants, with CD cludes cells that produce acid, mucus, epithelial barriers prevent absorption of
have appeared in the literature for years. antibodies, and other substances that more than 99% of the proteins in the in-
A conference convened by the National protect the host from foodborne testinal tract (Newby, 1984). These epi-
Institutes of Health Division of Micro- pathogens (Burke, 1985). Food enter- thelial lining cells are constantly re-
biology and Infectious Disease (NIH/ ing the mouth is chewed, breaking it newed to ensure that damaged villi do
DMID, 1998) and the European Com- into smaller pieces and mixing it with not provide a location vulnerable to in-
mission’s Scientific Committee on Ani- saliva. When swallowed, the food trav- fection. The continued movement of the
mal Health and Animal Welfare (EC, els via the pharynx and esophagus to gut contents also keeps the microbial
2000) concluded that there is insuffi- the stomach. Upon entering the stom- populations (microflora) in the small
cient evidence to prove or disprove that ach, the food is broken down by gastric intestine at lower levels compared to the
M. paratuberculosis is the cause of CD. juices that contain pepsin, lipases and large intestine microflora, which exists
Studies to determine how M. paratuber- acids. in a more static environment.
culosis could be transferred from ani- From the stomach, the partially di- Digestive secretions are another ma-
mals to humans have focused on milk gested food enters the small intestine. jor form of nonspecific immunity in the
and results have been conflicting The intestine is approximately 20 feet GI tract. For example, the high acidity
(CAST, 2001). Both the NIH/DMID long and has an irregular, folded lining and pepsin content in the stomach work
conference and the EC committee rec- that provides a very large surface area to destroy microbial pathogens and their
ommended further study of this issue. that facilitates digestion and absorp- toxins. Enzymes in bile acids and pan-
An association between IBD and the tion of nutrients. It also facilitates ex- creatic secretions also can protect
bacterial L-forms of Pseudomonas, My- posure to microorganisms that sur- against microbial pathogens. Gastric
cobacterium, Enterococcus faecalis and vived passage through the stomach. and intestinal epithelia are covered by a
E. coli also has been suggested (Her- The tissues immediately below the epi- moving layer of continually replaced
man-Taylor et al., 2000; Korzenik and thelial lining cells contain blood capil- mucus, a protein that contains sugar
Dieckgraefe, 2000). laries to absorb monosaccharides and residues to protect against proteolytic at-
The preceding examples are repre- amino acids and deliver bloodborne tack and microbial attachment. In addi-
sentative, but they do not present a com- defenses, and lymph capillaries to ab- tion to functioning as a lubricant and
prehensive discussion of foodborne dis- sorb fatty acids and glycerol. Enzymes protecting the stomach and intestine
ease. The differing symptoms, duration and hormones secreted by the liver and from acidic pH, the mucus is a vehicle
and severity make diagnosis and com- pancreas assist digestion and absorp- for antibacterial substances (e.g., secre-
prehensive tracking of foodborne illness tion in the small intestine. Because of tory immunoglobulin A and enzymes)
difficult. The large number of foodborne its length, surface area (equivalent to a and prevents large molecular weight ma-
pathogens—each with its own virulence singles tennis court), and digestive ca- terials from passing into enterocytes, the
factors—produce an astonishing array pacity, more than 80% of absorption epithelial lining cells.
of illnesses, and the pathogens continue occurs in the small intestine. Undigest- As a stable ecosystem, the normal in-
to evolve. Millions of illnesses and thou- ed food material enters the large intes- testinal microflora diminish opportuni-
sands of deaths occur each year as a re- tine (colon), through which it travels ties for pathogenic microbial infection.
sult of contaminated food in developed until it finally exits the anus. Anatomic, By occupying the available binding sites
countries, and the situation is much physiologic, and pathologic changes in on the enterocytes, decreasing the pH of
worse in the developing world. the GI tract influence the level of pro- the gut lumen, producing volatile fatty
tection from the effects of pathogens. acids and selective antibiotics known as
Resistance to Microbial These GI tract changes also affect the bacteriocins, and increasing motility of
Foodborne Disease population of nonpathogenic microor- the gut contents, these nondisease-caus-
ganisms living in the GI tract, which ing (commensal) microbes provide an
Humans are protected from infec- influences the likelihood of foodborne important element of the nonspecific
tious foodborne disease by a variety of infections. defense system.
nonspecific (innate) and specific im- The large surface area, presence of Microbial agents or antigens that
mune system mechanisms. When all of large amounts of nutrients, and ab- manage to penetrate the epithelial barri-
these systems are functioning optimally, sorptive capacity of the alimentary ca- er may encounter mononuclear phago-
the chance of foodborne illness is re- nal make it particularly prone to pene- cytes (blood monocytes or tissue mac-

rophages) and polymorphonuclear ph- because they are multivalent, meaning ble for humoral immunity (antibody
agocytes (PMNs or granulocytes) that they have more than one chemical struc- production) and carry immunoglobu-
defend the rest of the body from things ture that can be recognized by the im- lins (antibodies) on their surface. T lym-
that get through the superficial defenses. mune system. phocytes can have both effector and reg-
PMNs, a primary defense against infec- Specific responses can be functional- ulatory functions. T cells control the
tious agents, can travel via blood vessels. ly divided into phases: (1) recognition, maturation of both effector T and B
Macrophages travel to an inflamed site (2) activation, and (3) effector (Abbas et cells. T cells also are involved in cell-me-
where they attempt to kill the intruder. al., 1997). In the recognition phase, for- diated immune responses such as cyto-
Certain blood proteins also can serve as eign antigens bind to specific receptors toxicity and delayed-type hypersensitivi-
backup nonspecific defense mechanisms on existing lymphocytes. Lymphocyte ty. Some B and T cells reside in specific
(Pestka and Witt, 1985). Interferon recognition of specific antigens triggers areas in the “secondary” lymphoid or-
formed by virus-infected cells can inhibit the activation phase. Activation events gans such as the spleen and gut-associat-
replication of unrelated viruses. Kinins include development of antigen-specific ed lymphoid tissue (GALT) to facilitate
are a group of peptides which, when acti- lymphocytes and a shift from recogni- contact between lymphocytes and circu-
vated, are involved in inflammation and tion to defensive functions. In addition lating antigens.
blood clotting. Finally, the complement to antigens, activation requires “helper” In addition to B and T cells, accesso-
system, a series of proteins and enzymat- or “accessory” signals from other cells. ry cells (macrophages, monocytes, and
ic reactions, can destroy invading cells. Finally, the effector phase implements an dendritic cells) can ingest and destroy in-
The nonspecific mechanisms de- active defense based on antigen recogni- fectious particles and function in antigen
scribed here act together to prevent infec- tion and lymphocyte activation. presentation that influences the strength
tion by enteric microorganisms or entry The immune system has numerous and type of antibody response. Mast cells
of large microbial toxins. Thus, under possible effector responses to an antigen- can respond to various antigens and
normal conditions, relatively large num- ic stimulus. First, one or more compo- generate a hypersensitivity response.
bers of microorganisms would be re- nents of the specific immune system can Mononuclear cells known as “killer” cells
quired for a few to survive the defenses work to remove the antigen. Second, spe- can bind to antibodies and facilitate lysis
and initiate infection. A variety of factors cific and nonspecific immune mecha- of tumor cells and cells infected with vi-
may depress nonspecific immunity, such nisms can interact to enhance the host’s ruses. Other cell types with the ability to
as decreased gastric acidity caused by in- ability to kill invading microorganisms. spontaneously dissolve or disintegrate
gestion of antacids, diminished native Third, an antigenic stimulus can induce neoplastic cells have been called natural
microflora following treatment with an- “tolerance,” which is a “specific” type of killer (NK) cells.
tibiotics, or damage to the epithelial bar- unresponsiveness. Thus, a host can rec- Gut-Associated Lymphoid Tissue
riers. When nonspecific immunity is de- ognize and tolerate the host’s own pro- (GALT). Differentiating generalized sys-
pressed, the likelihood that small num- teins, known as self antigens. The ability temic immunity from mucosal immuni-
bers of a pathogen will cause an infec- of the immune system to develop a ty is useful. The systemic immune system
tion is increased. However, even when in- memory allows the host to both prevent includes all the tissue involved in pro-
nate protection fails, specific defense future reinfection by an invading organ- tecting the body’s interior from invading
mechanisms can prevent infection and ism and to avoid mounting a self-de- microorganisms. The mucosal immune
disease. structive immune response. system consists of the lymphoid tissue
Cells of the Immune System. Many that borders the external environment of
Specific Immune Mechanisms highly specialized cells carry out the crit- the gut lumen or other sites such as the
ical functions of specific humoral (anti- lungs and nose. While this classification
In addition to the nonspecific im- body-mediated) and cell-mediated im- is helpful in analyzing diverse functions,
mune defenses described above, ingested mune reactions that influence a host’s re- many of the specific activities of lym-
microbes face other compounds that cir- sistance to infection and serious disease. phoid tissue in the systemic and mucosal
culate in the blood or are secreted into These cells are derived from stem cells in compartments overlap and can affect the
the lumen of the GI tract that are specific the bone marrow and become the lym- function of each other.
to certain microbes or related groups of phocytes, granulocytes, macrophages, GALT is made up of aggregated and
microbes. This “acquired” immunity rec- dendritic cells and other specialized pro- non-aggregated tissue (Elwood and Gar-
ognizes characteristics or components of tective cells during a process called he- den, 1999). The aggregated component
the microorganism, called antigens, and matopoiesis. To be responsive to the includes mesenteric lymph nodes, lym-
then inactivates, removes or destroys the present needs of the immune system, phoid nodules, and groups of nodules
microorganisms that possess these anti- many aspects of leukocyte development called Peyer’s patches that occur right un-
gens. To do this, the immune system are regulated by cell-to-cell interactions der the epithelial cells that line the lumen
must be able to recognize small differ- and by cytokines, soluble protein factors of the intestine. These sites contain a full
ences in the chemical structure of an an- that influence cell growth, differentiation complement of the immune cells neces-
tigen and “remember” these chemical and maturation. In most cases, the cell sary to launch an immune response. The
structures for long periods of time. Anti- types involved in generalized systemic non-aggregated tissue includes lympho-
gens are typically high molecular weight immunity also play key roles in gas- cytes, macrophages, and mast cells in the
(>10,000 Daltons) proteins or polysac- trointestinal immunity. lamina propria (connective tissue beneath
charides. Parts of the pathogen—such as Lymphocytes carry out critical regu- the epithelium) and the intraepithelial
the cell wall, flagella, capsule and tox- latory and effector activities in specific lymphocytes in the gut wall.
ins—serve as excellent antigens, in part immunity. B lymphocytes are responsi- Antigen Uptake in the Gut. In gener-


al, large molecules in the lumen of the system, sIgA is able to inhibit entry of the GI defensive barriers depends on sev-
intestines are digested into small compo- soluble antigens and restrict epithelial eral factors, such as the number of mi-
nent parts before they are absorbed. colonization by bacteria and viruses. croorganisms and virulence factors (see
However, high molecular weight antigens Specific Cell-Mediated Responses in virulence, p. 15). Thorne (1986) outlined
can move from the gut lumen into the the Gut. Cytotoxic T cells also can defend five pathogenic mechanisms for bacterial
blood. Prior to uptake, the antigens must a host against living antigens, such as vi- diarrheal diseases: (1) bacteria produce
resist proteolytic activity in the lumen rally infected cells or intracellular patho- toxin but do not generally adhere and
and penetrate the mucus layer so they gens. In such a response, a target host cell multiply (e.g., B. cereus, S. aureus, C. per-
can interact with the various absorptive bearing an antigen of the pathogen on its fringens, C. botulinum); (2) bacteria ad-
cell types. Factors that disrupt the mu- surface interacts directly with a cytotoxic here to the lining of the intestine and
cosal barrier function and facilitate the T cell resulting ultimately in the lysis of produce toxin (e.g., enterotoxigenic E.
uptake of antigens include immature the target cell. The killing is unidirection- coli, Vibrio cholerae); (3) bacteria adhere
gastrointestinal function, malnutrition, al and thus cytotoxic T cells can kill nu- and damage the villi that make up the
inflammation, and immunoglobulin de- merous target cells. brush border (e.g., enteropathogenic E.
ficiencies (Walker, 1987). At least two dif- The Common Mucosal Immune Sys- coli); (4) bacteria invade the mucosal lay-
ferent mechanisms may result in uptake tem. It appears that antigenic stimulation er and initiate intracellular multiplica-
of these macromolecules (Stokes, 1984). in the gut may result in IgA secretion at tion (e.g., Shigella spp.); and (5) bacteria
In the first, the intestinal epithelial cell other mucosal sites such as salivary penetrate the mucosal layer and spread
can incorporate macromolecular aggre- glands and genitourinary sites, leading to to lamina propria and lymph nodes (e.g.,
gates through endocytosis and deliver the concept of a “common mucosal im- Yersinia). With each increasing level of
these to the subepithelial space by exocy- mune system” (McDermott and Bienen- action, the pathogen’s focus moves from
tosis (Walker, 1987). In the second, anti- stock, 1979). While primarily demon- the mucosal to the systemic compart-
gens can be deliberately “sampled” by the strated in experimental animals, evi- ment, and, hence, the specific immune
specialized epithelial cells (M cells) that dence exists for a common mucosal im- response must escalate.
cover Peyer’s patches, which bring the in- mune system in humans, based on detec- The antigen-sampling process itself
tact antigen into the underlying lym- tion of gut antigen-specific IgA at ana- may become a major portal of entry for
phoid tissue to trigger a comprehensive tomically remote sites. Furthermore, an- pathogens (Owen and Ermak, 1990).
specific immune response. tigen-specific IgA producing cells can be Wells et al. (1988) hypothesized that, in
Specific Humoral Responses in the found in blood following oral immuni- some instances, a motile phagocyte may
Gut. Humoral immunity is mediated by zation and preceding their appearance in ingest an intestinal bacterium, transport
highly specific proteins known as anti- saliva and tears (Russell et al., 1991). The it to an extraintestinal site, fail to accom-
bodies, which are secreted in response to advantage of a common mucosal re- plish intracellular killing, and then liber-
the antigen that originally stimulates the sponse relates to the mobilization of hu- ate the bacterium at the extraintestinal
antibody formation. Antibodies are moral and cellular immune elements to site. This hypothesis was based on the
sometimes called immunoglobulins various sentinel sites (e.g., mouth, eye, observation that the intestinal bacteria
(Igs). There are five major classes or “iso- genitourinary tract) that can prevent in- that most readily translocate out of the
types” of immunoglobulins, each of fection at all of these sites upon subse- intestinal tract are facultative intracellu-
which functions slightly differently. Of quent reexposure to the pathogen. lar pathogens. Secondly, intestinal parti-
these, IgA is of predominant importance Stimulation of Specific Gut Immunity. cles without inherent motility (e.g., yeast,
in local immunity in the gut because Stimulating the specific immune response ferritin, starch) move out of the intesti-
much of it is secreted into the gut lumen within the gut to protect against various nal lumen within hours of their inges-
where it can interact with microorgan- microbial illnesses helps prevent disease. tion. Thirdly, the rate of translocation of
isms before they invade deeper into the However, achieving long-term memory intestinal bacteria can be altered with
body. In fact, IgA accounts for 60% of to- when immunizing orally is difficult be- agents that modulate immune functions
tal daily antibody production in humans cause ingested antigens tend to be degrad- such as phagocytosis. Thus, systemic in-
(McGhee et al., 1992). IgA is found both ed by acidic pH and proteolysis in the gut fection by translocating intestinal bacte-
in mucus secretions (secretory IgA or (Stokes, 1984). Oral immunization with ria could be a result of the antigen-sam-
sIgA) of the gut and as a circulating Ig. live organisms is generally more effective pling process that evolved to regulate the
Antigens in the gut, including those on than nonreplicating organisms for induc- immune response to intestinal antigens.
microbes, are most likely to encounter tion of IgA responses, implying that colo-
sIgA before any other Ig. Peyer’s patches nization and/or replication in the GI tract Low Molecular Weight Toxins
are usually considered to be the source of is required (McGhee et al., 1992). Further-
most IgA. more, particulate antigens function much As discussed above, high molecular
Primary roles that have been suggest- more effectively than soluble ones. Thus, weight toxins (proteins, polysaccharides)
ed for sIgA are antigen exclusion, inhibi- close contact with key components of the produced by microbes are cleared by the
tion of adherence of microorganisms, in- gut is required to induce a GI immune re- immune system. However, the immune
tracellular virus neutralization and ex- sponse. system does not respond to low molecu-
cretion of IgA immune complexes. Secre- Responses to Infectious Microbes. lar weight, nonpolar compounds, such as
tory IgA induces antigen removal by tak- Many different bacteria, parasites and vi- mycotoxins, which can be rapidly ab-
ing advantage of the normal clearing ac- ruses cause gastroenteritis or penetrate sorbed through the gastrointestinal tract.
tivities of the gut (Newby, 1984). Thus, the gut as an entry point to cause sys- Higher vertebrates have developed the ca-
working with the nonspecific immune temic infection. The capacity to override pacity to metabolize mycotoxins and oth-

er foreign materials (xenobiotics) via a Although biotransformation is an im- croorganisms. Susceptibility to infectious
process known as biotransformation (de portant mechanism of host defense, in disease is increased by conditions that al-
Bethizy and Hayes, 1994). The liver is the some cases, biotransformation can make ter the host defenses and suppress the
primary organ of xenobiotic biotransfor- xenobiotics more toxic. Notably, aflatoxin function of the immune system. Altered
mation because of its size and its central B1 is converted to a reactive epoxide that host defenses and immunosuppression
location in systemic circulation. However, can react with nuclear DNA and cause can be caused by an infection, another
specific limited biotransformation capaci- mutations that ultimately result in liver disease, aging, poor nutrition, or certain
ties can be found in other tissues and in cancer, although the original mycotoxin medical treatments (see Table 6). These
the microflora of the intestine. chemical structure is not carcinogenic. factors have all been implicated in the in-
Biotransformation can be divided creased risk of infection or increased se-
into two distinct phases. Phase I reactions Susceptibility to Microbial verity of illness caused by many food-
add specific functional groups to the toxin Foodborne Disease borne pathogens including Cryptospo-
that are used for subsequent metabolism ridium, Toxoplasma, Campylobacter, Sal-
by phase II enzymes. Phase II reactions The extent to which the human host is monella, L. monocytogenes, and Giardia
are considered biosynthetic. Biotransfor- susceptible to disease influences the likeli- (see sidebar, p. 35).
mation changes hydrophobic toxins to hood of foodborne illness. Many factors As described above, humans possess a
more polar, readily excreted compounds. play a role in the level of susceptibility. number of general and specific host de-
Examples of phase I reactions include ox- fenses against foodborne disease. General
idation, reduction, hydration, and hydrol- Infectious Disease defenses include normal indigenous mi-
ysis. Examples of phase II reactions in- croflora, the acidic pH of the stomach,
clude glucuronidation, sulfate conjuga- Susceptibility to infectious disease is and the antibacterial effect of the various
tion, glutathione addition, methylation, the inability of the host’s body to prevent pancreatic enzymes, bile and intestinal se-
and acetylation. or overcome invasion by pathogenic mi- cretions. The constant movement of the
intestine (peristalsis) helps maintain the
balance of normal flora and purge the in-
Table 6. Factors That Increase Host Susceptibility (adapted from CAST, 1994) testinal tract of harmful microorganisms.
General Factors that alter these general parameters
Factors Specific Factors Reasons can increase susceptibility to infection.
For example, Salmonella infection is more
Age Age less than 5 years Lack of developed immune systems, common in patients with decreased stom-
smaller infective dose-by-weight
ach acidity from medication or after gas-
trectomy. Slowing peristalsis with bella-
Age greater than 50 or 60 years Immune systems failing, weakened donna or opium alkaloids prolongs
(depending on pathogen) by chronic ailments, occurring as symptoms of shigellosis. Similarly, treat-
early as 50 to 60 years of age ment of typhoid fever with antibiotics
Sensitive Pregnancy Altered immunity during pregnancy prolongs the carrier state for Salmonella
populations Typhi, and some evidence indicates that
Hospitalized people Immune systems weakened by other antibiotic treatment of E. coli O157:H7
diseases or injuries, or at risk of increases the risk of HUS. Additionally,
exposure to antibiotic-resistant
altering the bowel microflora with broad
spectrum antibiotics can lead to over-
Possession of certain human antigenic Predisposition to chronic illnesses growth of pathogenic organisms (e.g., Sal-
determinants duplicated or easily (sequelae) monella).
mimicked by microorganisms In the United States, end-stage can-
Underlying Concomitant infections Overloaded or damaged immune cer, renal disease, end-stage AIDS, liver
medical systems disease, and alcoholism are the most
conditions common underlying illnesses that di-
Consumption of antibiotics Alteration of normal intestinal minish cellular immune response. Im-
microflora munosuppression often accompanies
Excessive iron in blood Iron in blood serving as nutrient for drug or radiation therapy. Corticoster-
certain organisms oids, chemotherapeutic agents used in
cancer and organ transplantation, and
Reduced liver/kidney function Reduced digestion capabilities,
total lymphoid irradiation all suppress
(alcoholism) altered blood-iron concentrations
the cell-mediated immune (CMI) func-
Surgical removal of portions of stomach Reduction in normal defensive tion. Organ transplant patients receiving
or intestines systems against infection combined immunosuppressive therapy
Immunocompromised individuals Immune system inadequate to (corticosteroids, azothiprine, and cy-
including those on chemotherapy or prevent infection closporin) face an increased risk of in-
radiation therapy; recipients of organ fection (or reactivation of quiescent in-
transplants taking immunocompro- fections) with a variety of opportunistic
mising drugs; people with leukemia, pathogens including L. monocytogenes,
AIDS, or other illnesses Salmonella, T. gondii, Cryptosporidium,


Cryptosporidium was first de- posure to infected calves. While these of water distributed by one of two wa-
scribed in the early 1900s but was not patients typically had self-limited illness- ter treatment plants in Milwaukee
considered to be medically or eco- es of mild severity, they demonstrated (MacKenzie et al., 1994).
nomically important. During the ear- that calves with diarrhea were a potential Cryptosporidiosis is now recog-
ly 1970s, Cryptosporidium was linked source of human infection. The second nized as an important cause of diar-
to diarrhea in calves, and case reports observation was the occurrence of rheal illness, and is estimated to cause
describing its appearance in a variety chronic protracted diarrhea due to 300,000 illnesses each year in the Unit-
of animal species began to appear in Cryptosporidium in patients with ac- ed States (Mead et al., 1999). Geno-
the literature. In 1976, Cryptosporidi- quired immune deficiency syndrome typing methods have been developed
um was first associated with severe (AIDS). In many of these patients with to discriminate between strains of hu-
watery diarrhea in a patient who had severe cell-mediated immune defects, man and bovine origin, although hu-
been receiving immunosuppressive cryptosporidiosis was unresponsive to mans are susceptible to infection with
chemotherapy for 5 weeks. The diar- therapy and culminated in death (Navin bovine strains. Application of these
rhea resolved 2 weeks after discontin- and Juranek, 1984). methods to outbreak investigations
uation of the therapy. Following this During the mid-1980s, the first out- and surveillance data will improve our
report, additional case reports of se- breaks of cryptosporidiosis in child day understanding of the epidemiology of
vere, persistent diarrhea in immuno- care centers and the first waterborne out- cryptosporidiosis. Interestingly, al-
suppressed or immunodeficient indi- breaks of cryptosporidiosis were reported. though manure runoff from dairy
viduals appeared in the literature (Pit- As clinicians and laboratories became farms and effluent from beef slaughter
lik et al., 1983). more aware of Cryptosporidium, its role as plants were suspected to be likely
During the early 1980s, two series a cause of community-acquired diarrhea sources for the Milwaukee outbreak,
of observations began to shape the emerged. This growing awareness of the Cryptosporidium oocysts recovered
emerging epidemiology of human public health importance of cryptospo- from outbreak-associated cases were
cryptosporidiosis. First, cases of ridiosis culminated with the occurrence of of the human genotype (Sulaiman et
cryptosporidiosis were reported a massive waterborne outbreak in Mil- al., 1998). Thus, effluent from a plant
among persons who had normally waukee, Wis., in 1993. More than 400,000 treating human waste was a more like-
functioning immune systems and ex- illnesses were attributed to contamination ly source.

and Trichinella spiralis. In one study, in- dence rates of Shigella infection 30 times immune function with age, termed “im-
dividuals with chronic heart disease had greater than the HIV-free population mune senescence.” The data regarding the
an increased risk for listeriosis (Schuchat (Baer et al., 1999), and using an immune effects of aging are confusing and some-
et al., 1992). Cellular immunity declines suppressive medication was identified as a times conflicting. In general, cell-mediated
during pregnancy, which may account risk factor for sporadic E. coli O157:H7 immunity declines, including both func-
for the severity of certain infections. infections in a FoodNet case-control tional and quantitative cell counts. Su-
Evidence indicates that immune defi- study (Kassenborg et al., 1998). perimposed and interrelated with this
ciency not only increases the number of It is known that the neonatal, pediat- generalized impairment are age-related
cases but also the severity of infection ric, adult, and elderly immune systems decreases in organ structure and function.
from a wide variety of foodborne patho- differ. The fetus and neonates are highly Nutritional abnormalities in macro- and
gens. For example, studies conducted in susceptible to infection with a variety of micronutrients are common in the elderly
Los Angeles, San Francisco and New pathogens, presumably as a result of an and may compound immune senescence.
York City during the mid-1980s demon- immature immune system. The develop- The presence of other illnesses and envi-
strated that patients with acquired im- ment of the immune system begins early ronmental factors also may contribute to
mune deficiency syndrome (AIDS) had in fetal development, but children are not the decline.
rates of Campylobacter and Salmonella immunologically mature until puberty,
infection that were 19 – 94 times the gen- putting them at increased risk for food-
Susceptibility to Biotoxins
eral population rates in the same cities borne illness.
(Celum et al., 1987; Greunewald et al., Improvements in health care and nu- The variability of human susceptibil-
1994; Sorvillo et al., 1994). In addition, trition in this century have increased the ity to mycotoxins and other biotoxins can
16% of Campylobacter infections and life expectancy for most people. One re- be attributed to physiologic and environ-
44% of Salmonella infections resulted in sult is that the elderly are the fastest-grow- mental factors, host genetics, and the pres-
bacteremia in these compromised pa- ing segment of our population. Elderly ence of infection and inflammation.
tients, much higher rates of severe dis- people experience significantly greater
ease than occurred in the general popu- morbidity and mortality from infectious
Physiologic Factors
lation. San Francisco residents infected diseases than the general population. This
with the human immunodeficiency virus apparent susceptibility to infection in the A number of factors can influence a
(HIV) also have been shown to have inci- elderly has been attributed to a decline of person’s ability to detoxify ingested

biotoxins. For example, biotransfor- valenol due to leukocyte cell death (Zhou throughout the world’s developed coun-
mation enzyme activity can vary dur- et al., 1999; 2000). tries. Schools, education programs, me-
ing perinatal and postnatal develop- dia communications, and the Internet
ment (deBethizy and Hayes, 1994). Other Factors have made foodborne and waterborne
When the individual is older, environ- diseases important concerns to many
mental forces play a role in host re- Other significant host factors, apart consumers. Outbreaks of foodborne ill-
sponse: the nutritional quality of the from immune suppression per se, are as- ness that would have gone unnoticed a
diet, the presence of chemicals in the sociated with increased risk of both acute decade ago are now the subject of rapid,
diet, and the intake of prescription or foodborne disease and chronic sequelae. in-depth news coverage. The increased
elicit drugs can affect the profile of Genetic predisposition and underlying publicity about infectious foodborne
biotransformation enzymes. Finally, chronic disease have been cited as poten- hazards appears to reinforce food safety
environmental toxins in air (e.g., ciga- tial risk factors. For instance, septic messages and to increase motivations to
rette smoke) and water can increase or Vibrio vulnificus infections are most handle foods safely.
decrease the activity of biotransforma- commonly seen in men over 50 years of Proper hygiene and sanitation related
tion enzymes toward specific mycotox- age with liver and/or blood disorders to food handling and preparation, ap-
ins or other biotoxins. (Desenclos et al., 1991; Tacket et al., propriate methods of refrigeration and
1984). These underlying conditions fre- freezing, and thorough cooking of foods
Genetic Polymorphisms quently result in elevated serum iron lev- comprise a very effective approach to
els that play a role in V. vulnificus disease preventing foodborne illness. However,
Wide differences in the human ca- pathogenesis, although the exact mecha- these behaviors are just one aspect of a
pacity to biotransform biotoxins appear nism is not fully understood (Wright et healthy life-style. Additional behavioral
to relate to genetic background that in- al., 1981). Similar evidence is available changes—such as consuming probiotics,
fluences the presence, amount and acti- for yersiniosis in iron-overloaded pa- eating a balanced diet, and exercising
vation of various enzyme systems that tients treated with deferioxamine, al- regularly to maintain a healthy weight—
metabolize ingested biotoxins into chem- though again the pathogenic mecha- foster proper functioning of the immune
ical derivatives that are less or sometimes nisms are not yet clear (Mandell and system that may heighten resistance to
more toxic than the original mycotoxin Bennett, 1995). As previously discussed, occasional pathogens in the food supply.
(Daly et al., 1994; Kalow, 1993). For ex- genetic predisposition plays a role in the Consumer awareness of food safety
ample, the level of expression for development of chronic reactive arthritis. issues has placed additional pressure on
CYP1A2, a cytochrome P-450 (CYP)-de- Recent evidence from a quantitative hu- the food service and food processing in-
pendent monooxygenase that metaboliz- man challenge study for the Norwalk- dustries to improve their efforts to en-
es aflatoxin B1 varies considerably in the like virus indicates a two-phase dose-re- sure the safety of the products they pro-
human liver (Eaton et al., 1995). The ac- sponse relationship that appears to be vide both domestically and internation-
tivity of microsomal epoxide hydrolase, separately associated with prior exposure ally. Hazard Analysis and Critical Con-
which acts coordinately with CYP1A2, (antibody titer) and individual suscepti- trol Points (HACCP) implementation
can vary up to 40-fold in human tissue bility, neither of which are associated has become commonplace in the food
(Seidegard and Ekstrom, 1997). It has with any recognized specific host factors processing and delivery process. Com-
been suggested that epoxide hydrolase (Moe et al., 1999). When taken together, panies have a strong economic incentive
polymorphisms may alter the risk this body of evidence suggests that many to prevent outbreaks of foodborne ill-
of aflatoxin-associated liver cancer factors apart from immune suppression ness associated with their product or res-
(McGlynn et al., 1995). Specifically, en- influence host susceptibility to food- taurant.
zymes may vary in both the amount borne disease agents. While many host factors that influ-
present and their effectiveness/activity, ence infection, occurrence and severity
resulting in differing risks of a negative Individual Choices that Affect of illness are associated with human
outcome from aflatoxin ingestion. Disease Risk physiology, the factors that influence ex-
posure to foodborne pathogens are often
Infection and Inflammation Which foods are consumed and how tied to human behavior, specifically con-
those foods are prepared affect an indi- sumption, food handling, and prepara-
The simultaneous presence of an in- vidual’s risk of foodborne disease. De- tion behaviors.
fectious microbe with attendant inflam- spite education efforts, consumer behav- Eating outside the home in restau-
mation can increase the sensitivity of a ior continues to play a significant role in rants and other foodservice venues has
host to mycotoxic disease. Epidemiolog- exposure to foodborne pathogens (see been identified as a risk factor for certain
ic studies have demonstrated that hepati- Table 7). foodborne diseases (Friedman et al.,
tis B infection predisposes humans who 2000), and the number of meals that
chronically ingest aflatoxins to develop Behavior Changes Americans eat away from home contin-
primary liver cancer (Pitt, 2000). In ex- ues to increase. In the 1990s, food eaten
perimental animals, gram-negative bac- The 1990s saw a tremendous increase outside the home accounted for almost
terial endotoxin can cause a predisposi- in public awareness of food safety issues 80% of reported foodborne illness out-
tion to acute liver injury from aflatoxin in the United States. This awareness breaks in the United States (Bean et al.,
B1 (Barton et al., 2000, 2001) and T-2 arose in part because of the continuing 1996). Because of the larger number of
toxin (Tai and Pestka, 1988) and to de- interest in personal health and well be- people involved, these outbreaks are
pletion of lymphoid tissue by deoxyni- ing, a phenomenon that occurred more likely to be recognized and, there-


Table 7. Factors That Increase Risk of Foodborne Disease (adapted from CAST, 1994) both in school and at home. Health edu-
cators in secondary schools emphasize
General prevention of other important health
Factors Specific Factors Reasons
concerns (e.g., HIV infection, obesity)
Life-style Stress Body metabolism changes, allowing over consumer safety issues including
easier establishment of pathogens, or food safety education (Collins et al.,
lower dose of toxin required for illness 1995). In addition, the trend toward two-
Poor hygiene Increased likelihood of ingestion of
income families and eating away from
pathogens home leaves fewer opportunities to pass
food safety information from parent to
Geographic location Likelihood of exposure of endemic virulent child (Manchester and Clauson, 1995).
strains; limited and/or compromised food Travel, another factor in foodborne
and water supply; variable distribution of illness, has increased dramatically during
organisms in water and soil
the 20th century. Five million interna-
Diet Nutritional deficiencies either through Inadequate strength to build up resistance tional tourist arrivals were reported
poor absorption of food (mostly ill or and/or consumption of poor-quality food worldwide in 1950, and the number is
elderly people) or unavailability of ingredients, which may contain pathogens expected to reach 937 million by 2010
adequate food supply (starving people) (Paci, 1995). Travelers may become in-
Consumption of antacids Decreased stomach acidity (increased pH) fected with foodborne pathogens un-
common in their nation of residence,
Consumption of large volume of liquids Dilution of acids in the stomach and rapid thus complicating diagnosis and treat-
including water transit through the stomach ment when their symptoms begin after
Ingestion of fatty foods (such as Protection of pathogens against stomach they return home. In 1992, for example,
chocolate, cheese, hamburger) an outbreak of cholera caused 75 illness-
containing pathogens es in international airline passengers; 10
persons were hospitalized, and one died
(Eberhart-Phillips et al., 1996). Patho-
gens also may be carried home and infect
fore, reported to health officials, so the dling raw meat (Altekruse et al., 1995). family members and other close personal
extent of the role of foodservice in food- As many as 42% of survey respondents contacts (Finelli et al., 1992).
borne disease may be overstated. None- did not cook hamburgers at home until
theless, the role of foodservice has be- well done (Albrecht, 1995). In a 1992 Changes in Food Consumption Behavior
come more significant as the percentage study, 23% of respondents reported eat-
of the food budget spent on eating out ing raw shellfish (Timbo et al., 1995). Potential exposure to pathogens is
has increased during recent decades Fortunately, some high-risk food-han- not only a function of how food is han-
(Manchester and Clauson, 1995). dling and consumption behaviors, al- dled, but also what foods individuals
Quick-service restaurants and salad bars though still common in 1995 and 1996, choose to eat. Similar to the link between
were rare 50 years ago but are primary did show improvement (CDC, 1998a). poor sanitation practices and foodborne
sites for food consumption in today’s The reasons why some consumers illness, consumption of certain foods in-
fast-paced society (Manchester and respond to food safety information and creases the risk of illness.
Clauson, 1995). admonitions to choose safe food and Changes in food consumption have
Regardless of what has or has not handle it properly while other consumers brought to light previously unrecognized
happened to commodities on their way do not are poorly understood. Demo- or underestimated microbial hazards.
from farm to table, the final common graphic factors such as gender, age and Fresh fruit and vegetable consumption,
pathway for food involves storage, prepa- education level are associated with high- for example, increased nearly 50% from
ration, and serving prior to the time of risk behaviors. For instance, all behaviors 1970 to 1994 (BC/USDC, 1996). Produce
consumption. Unfortunately, foods that associated with increased risk of food- is susceptible to microbial contamina-
are free of foodborne pathogens and tox- borne diseases were more prevalent in tion during growth, harvest, and distri-
ins early in the food chain can become men than in women. (Albrecht, 1995; Al- bution (see section on microbial ecology,
unsafe if not handled properly during the tekruse et al., 1995). The 1993 FDA p. 40), which is of special concern for
final stages of preparation and service. Health and Diet Survey indicated that foods eaten fresh and not cooked. Patho-
Food handling behaviors such as in- men were less likely than women to wash gens on the surface of produce (e.g., mel-
adequate hand washing, unsafe storage their hands after handling raw meat or ons) can contaminate the interior during
temperatures that permit the growth of poultry (53% versus 75%) (Altekruse et cutting and multiply if the fruit is held at
low levels of pathogens, incomplete al., 1995). Results of several studies indi- room temperature (Reis et al., 1990). In
cooking of potentially hazardous foods, cate that younger people have a higher the United States from 1990 to 1997, a
and cross-contamination of fresh and prevalence of a number of risky food series of foodborne outbreaks were asso-
cooked foods are a problem whether they handling, preparation, and consumption ciated with produce such as sliced canta-
take place inside or outside the home. practices (Altekruse et al., 1995; Klontz et loupe (Reis et al., 1990), green onions
Based on data from a 1993 nationwide al., 1995; Timbo et al., 1995). Education (Cook et al., 1995), unpasteurized cider
survey, an estimated 37% of food han- efforts are complicated by decreased op- (Besser et al., 1993), fresh-squeezed or-
dlers did not wash their hands after han- portunities for food safety instruction ange juice (Cook et al., 1996), lettuce

(Ackers et al., 1996), raspberries (Her- ple juice or apple cider; 3.4% drank and leaner meats such as chicken. Recent
waldt, 1997), alfalfa sprouts (Mahon et unpasteurized milk; and 2.5% ate fresh increases in the consumption of health-
al., 1997), sliced tomatoes (Wood et al., oysters. promoting fresh fruits and vegetables
1991), and frozen strawberries (CDC, have resulted in increased likelihood of
1997a). Cultural Differences exposure to certain diseases like hepatitis
In addition to relative changes in A, shigellosis and salmonellosis from
quantities, the past few decades have Diet selection can create subpopula- contaminated produce (Tauxe et al.,
seen dramatic changes in the diversity tions at greater risk for certain food- 1997). The dietary shift toward increased
of foods available to the American pub- borne illnesses. Some reports of food- consumption of chicken may have con-
lic. The growing wealth of Americans borne illnesses involve transmission via tributed to the high incidence of C. jeju-
and the profitability of fresh produce foods consumed primarily by immigrant ni infection (Friedman et al., 1992),
has led to the introduction and in- groups. Outbreaks of trichinosis have which now exceeds Salmonella as the
creased availability of a wide variety of become relatively rare in the United most common bacterial cause of food-
produce items—from kiwi, mangoes States because cooking pork thoroughly borne illness (Mead et al., 1999). A recent
and papayas, to alfalfa sprouts, specialty has become a widespread cultural prac- study demonstrated that only 17% of
lettuces and fresh-cut, packaged pro- tice. An exception occurred in 1990, Americans ate five or more servings
duce. Imported produce has played a when Laotian immigrants in Iowa pre- of fresh fruits and vegetables per day
significant role in increasing diversity. pared and ate undercooked pork, a tradi- (Thompson et al., 1999). Thus, public
Fresh produce has also become a main- tional food, as part of a wedding celebra- health marketing campaigns are likely to
stay of restaurant fare; dinner salads tion (Stehr-Green and Schantz, 1986). increase fruit and vegetable consump-
and salad bars have become main- Other reports involve foods more com- tion in years to come.
stream. In addition, ethnic cuisines that monly consumed by ethnic populations. Medical and public health advisory
feature fresh produce ingredients, such Y. enterocolitica outbreaks are also rare, bodies also have advised certain subpop-
as Chinese, Mexican, Thai, and Middle but several outbreaks in African-Ameri- ulations to use special caution in diet se-
Eastern, have become popular. can communities were associated with lection and food preparation. For exam-
preparation and consumption of pig in- ple, the American Academy of Pediatrics
Individual Choices testines (Lee et al., 1990). The epidemiol- has recommended that children should
ogy of human brucellosis in California not drink unpasteurized milk or eat un-
Americans pride themselves on has shifted from an occupational disease pasteurized cheese, undercooked eggs,
their individual freedoms. In a culture related to animal husbandry to a food- raw or undercooked meat or meat prod-
based on these individual rights, we al- borne disease most frequently affecting ucts (AAP, 2000). FoodNet population
low people to engage in high-risk be- Hispanics who often consume raw milk surveys (CDC, 1999a) demonstrate that
havior and offer products that some- and cheeses made with raw milk while these types of dietary recommendations
times cater to these risks. Steps are tak- abroad (Chomel et al., 1994). Consump- do have an impact on consumer behav-
en to mitigate risk but ultimately cer- tion of rare hamburgers—a risk factor ior, although final analyses are not com-
tain behaviors are inherently risky. for E. coli O157 infection—is more com- plete. While 13.5% of adults aged 20-39
Sometimes people knowingly engage in mon in U.S. Caucasians than in any oth- who consumed hamburgers ate ham-
high-risk behavior. If people are aware er racial/ethnic group (CDC, 1998a). burgers that were pink, only 4.4% of
of the risks and continue to engage in children under 10 years of age did so.
risky behavior such as eating raw oys- Dietary Recommendations Similarly, adults were 2–3 times more
ters or eggs, it is appropriate to consid- likely than children to drink unpasteur-
er to what lengths our society should A host of organizations have issued ized milk, or eat alfalfa sprouts or runny
go to protect them. dietary recommendations and provided eggs (CDC, 1999a).
Surveys conducted from 1998-1999 information to assist in health promo- Ignoring recommendations about
as part of the FoodNet Active Surveil- tion and chronic disease prevention (U.S. preparation practices such as adequate
lance Program for foodborne diseases PSTF, 1997). These recommendations cooking places consumers at greater risk
have documented certain aspects of may advocate increased or decreased for foodborne illness. Consumer educa-
consumer behavior. With regard to consumption of certain types of foods, tion is an important part of foodborne
consumption of fresh produce that is outline specific circumstances for con- illness prevention. As the statistics above
known to be at particular risk for mi- sumption, or caution individuals with demonstrate, the media attention, safe
crobial contamination, 19% of respon- certain medical conditions. Each type of handling labels, public health advisories,
dents reported eating a mesclun lettuce recommendation has consequences for and public information and education
mix in the 7 days before the interview, foodborne illness. In recognition of the campaigns to date have left a substantial
and 8% reported eating alfalfa sprouts, importance of food safety, the latest edi- part of the population unprotected. For a
although these eating habits are highly tion of the federal government’s dietary variety of reasons, food safety and other
regional (CDC, 1999a). Among other guidelines contains a section on food public health messages fail to reach their
potentially risky food exposures, 25% safety. intended audience, are misunderstood,
of the people who had eaten eggs had Counseling the general population to or are disregarded. For those charged
chosen to eat eggs that were runny; limit dietary intake of fat and emphasize with preventing foodborne disease, there
11% of persons who consumed ham- foods containing fiber (i.e., fruits, vegeta- are two inescapable lessons in this data:
burgers ate burgers that were still pink bles, grain products) has increased con- first, we need to know a great deal more
inside; 4.4% drank unpasteurized ap- sumption of foods such as fresh produce about risk communication, education,


and motivation before consumer and mutants that have an impaired ability to fectious agents remains challenging be-
food worker education programs can be survive in vivo, and some of these have cause immunity is poorly understood,
considered credible parts of our overall been used as live oral vaccines to immu- the group has tremendous antigenic and
food safety strategy; and second, as long nize against subsequent infection with genetic diversity, and the viruses cannot
as pathogens are delivered to home and wild-type virulent strains (Fairweather et be cultivated in model animal or labora-
commercial kitchens, some foodborne al., 1990). An alternative vaccination ap- tory systems.
disease will occur. proach has focused on the use of puri-
fied antigens, although this usually re- Probiotics
Modification of Susceptibility sults in a comparatively poorer immune
response when administered orally (Fair- Probiotics represent another oppor-
Because of the significance of the hu- weather et al., 1990). tunity to use our understanding of the
man host in foodborne illness, it is ap- Scientists have had greater success gut microflora and the immune response
propriate to look for host-related oppor- developing effective vaccines against the to facilitate human health and decrease
tunities for control or mitigation of ill- human enteric viruses that are common- susceptibility to illness. Although origi-
ness. Certainly, behavioral and demo- ly spread through food and waterborne nally used to describe substances pro-
graphic issues influence susceptibility routes. For instance, we are in the final duced by one protozoan that stimulated
and exposure. If the host could be ren- stages of worldwide eradication of the another (Fuller, 1989), the definition for
dered immune to infectious agents, ill- poliovirus, an accomplishment made the term “probiotic” now generally im-
ness would cease to occur despite micro- possible by widespread immunization plies a viable microbial supplement that
bial contamination in the food supply. (Jacob, 2000). Vaccines for HAV are an- beneficially affects the host (human or
Although complete protection is current- other success story. Licensed in the mid- animal) by improving or maintaining a
ly out of reach for many pathogens, ap- 1990s, these vaccines consist of forma- desirable microbial balance in the gut.
proaches such as immunization and pro- lin-inactivated organisms and are well The reduction of harmful enteric micro-
biotics can decrease human susceptibili- tolerated; they produce durable immuni- organisms is only one of numerous po-
ty. Coupling these approaches with ef- ty persisting for more than 20 years tential health benefits of maintaining a
forts to mitigate exposure would further (Cuthbert, 2001). Recent evidence also healthy gut microflora. Probiotic cul-
boost our ability to control foodborne indicates that the HAV vaccine effectively tures are consumed in foods or capsules
illness of infectious origin. prevents secondary HAV infection and or are facilitated by ingesting prebiotics
may be appropriate for administration to (compounds that enhance the prolifera-
Immunization individuals in frequent personal contact tion of beneficial indigenous bacteria).
with infected persons, replacing the Currently, dairy foods such as yogurt
Vaccines use the host’s own immune widely used immunoglobulin (Sagliocca have been the most popular vehicle of
system to combat disease. Knowing how et al., 1999). Although there has been in- choice to deliver viable probiotic cul-
the immune system functions enables terest in mandating routine HAV vacci- tures. Intestinally-derived lactobacilli
scientists to investigate methods to en- nation for food handlers, there is cur- and bifidobacteria predominate in this
hance its effectiveness or trigger its pro- rently no overwhelming support for this role (Hughes and Hoover, 1991).
tective effects without causing illness. proposal, in part due to the expense of The effect of probiotic cultures varies
The medical community has had great this type of approach. Perhaps more effi- based on numerous conditions. The hu-
success with vaccination for some infec- cacious would be recommendation of man gut contains 100 trillion viable bac-
tious diseases, and potential vaccines to routine vaccination of individuals with teria and other microorganisms repre-
prevent foodborne illness are the subject underlying chronic active hepatitis due senting anywhere from 100 to 400 differ-
of considerable research. to infection with hepatitis B or C viruses, ent species; the population dynamics are
Although no vaccines are currently since this subpopulation is particularly quite complex. The microflora of the
available for most enteric bacterial susceptible to very serious disease mani- human intestinal tract is affected by ge-
pathogens, experimental approaches are festations if concurrently infected with netic or host factors, the composition of
under investigation. In general, vaccina- HAV. microbial populations, and the metabo-
tion strategies to control enteric bacterial In 1998, FDA also licensed a live at- lites produced by these microbes; these
diseases are complicated by many factors, tenuated rotavirus vaccine (Rotashield, factors are in turn influenced by climate,
not the least of which is the complexity Wyeth-Lederle Vaccines and Pediatrics, diet, stress, drugs, age, and disease (Mit-
of host immunity as well as a general ab- Philadelphia, Penn.) for oral administra- suoka, 1990). One can maintain that
sence of appropriate animal models for tion to infants (AAP, 1998). Unfortu- whenever there is a change in the intesti-
oral challenge and subsequent disease nately, in the summer of 1999, CDC re- nal microflora from its normal state, the
presentation for many of these patho- ported a clustering of cases of an intesti- change is detrimental or undesirable. A
gens. For example, an effective broad- nal complication in the weeks after vacci- foodborne intestinal infection that pro-
spectrum vaccine against enterohemor- nation, eventually leading to the volun- duces diarrhea can be viewed as a period
rhagic E. coli (EHEC) will likely need to tary withdrawal of the product from the of microbial imbalance or instability in
target systemic immunity against the U.S. market and an uncertain future for the gastrointestinal tract. However, by es-
Shiga toxins as well as local intestinal the vaccine (Weijer, 2000). Some tablishing themselves in the human GI
immunity against intestinal colonization progress has been reported in vaccina- tract in proportionally high numbers,
factors (Nataro and Kaper, 1998). None- tion against the human gastrointestinal acidulating bacteria, such as lactobacilli
theless, genetic manipulation has en- caliciviruses. However, protection against and bifidobacteria, may protect the gut
abled researchers to produce bacterial this important group of foodborne in- against invasive pathogenic agents.

Thus, regular consumption of foods acid-sensitive enteric pathogens, wheth- 100 years ago (Metchnikoff, 1908).
containing probiotics has a strong po- er the pathogens are indigenous to the More recent examples include Saavedra
tential to help maintain a beneficial and intestinal population or opportunistic et al. (1994), who showed that supple-
stable intestinal microflora that pro- contaminants of food and water (Lang- menting infant formula with Bifidobac-
motes intestinal health. This is especial- hendries et al., 1995). terium bifidum and Streptococcus ther-
ly true for those subpopulations with A similar case for administration of mophilus can reduce the incidence of
compromised or underdeveloped gut probiotic cultures would be for the new- acute diarrhea and rotavirus shedding
flora, such as the elderly, infants, and born (Mitsuoka, 1989). Within a day of in infants; Bernet et al. (1994), who
patients treated with antibiotics or che- birth, bacteria commence colonization found that consumption of a greater
motherapy. For example, in the elderly, and proliferation in the previously sterile number of lactobacilli provided in-
there is a steady decline in numbers of intestinal tract. Initially, coliforms, en- creased protection against cell associa-
bifidobacteria and an increase in the terococci, staphylococci, and clostridia tion by enterotoxigenic and entero-
numbers of C. perfringens with age. appear, but in three to four days after pathogenic E. coli and S. Typhimurium,
With this shift in gut flora, there is a birth, lactobacilli and bifidobacteria pre- and against cell invasion by entero-
corresponding increase in putrefactive dominate. Bifidobacteria soon dominate pathogenic E. coli, S. Typhimurium and
substances in the intestinal tract that are all other bacteria, whether the infant is Y. pseudotuberculosis; and Okamura et
inherently toxic and impose a constant breast-fed or bottle-fed. However, in bot- al. (1986), who used a tissue culture in-
stress upon the liver (Mitsuoka, 1990). tle-fed infants, populations of coliforms fection assay to demonstrate that ad-
In addition to C. perfringens, the putre- and enterococci are ten times higher than ministration of Bifidobacterium infantis
factive organisms that convert amino in breast-fed infants, a fact that may en- prohibited invasion and intracellular
acids into amines and other toxic sub- courage the use of infant formula that multiplication of S. flexneri. In all, pro-
stances include Salmonella, Shigella, and includes probiotic cultures. biotic cultures have demonstrated an
E. coli. As a means to ameliorate these The feeding of probiotic cultures to inhibitive or antagonistic effect against
detrimental conditions, elevated levels prevent or treat disease is well estab- almost all foodborne pathogens, includ-
of bifidobacteria and lactobacilli from lished in the scientific literature. Elie ing Salmonella, Shigella, E. coli, Campy-
dietary probiotics reduce fecal pH to Metchnikoff of the Pasteur Institute first lobacter, Clostridium, Yersinia, Vibrio
discourage growth and colonization by promoted the use of probiotics nearly and Candida (Fuller, 1992).

Microbial Ecology and Foodborne Disease

The complexity of the pre-harvest, Improved understanding of these food safety are broad concerns that apply
harvest, and post-harvest environ- complex factors provides insight into to many different commodities. Because
these issues affect so many commodities,
ments makes it impossible to control pathogen evolution and opens the door improvements in these areas would have
all potential sources of microbial to new and improved prevention and significant food safety impact.
contamination. Efforts at prevention control methods.
and control are implemented through-
Global Food Trade
out the food production and processing Globalization of the world’s food
PRE-HARVEST ENVIRONMENT supply has contributed to changing pat-
system. Researchers are continually
terns of food consumption and food-
searching for a better understanding of Efforts to minimize microbial con- borne illness. A growing percentage of
the pathogens and their interaction tamination of food begin in the pre-har- the U.S. food supply is imported. The
vest environment. Raw ingredients are sheer volume of these imports adds to
with the environment, leading to one way in which pathogens are intro- the complexity of foodborne illnesses.
improved control technologies. But at duced into the processing environment. Global sourcing provides economic
the same time, the pathogens continue Unfortunately, pathogen control in the benefits and a wider selection for con-
production agriculture environment is sumers that improves nutrition world-
to evolve, and human actions some- often difficult. wide. However, in terms of disease
times drive that evolution. Even small control programs, globalization mini-
environmental changes can have Overarching Issues mizes traditional geographic barriers
to emerging as well as traditional
unforeseen or even unforeseeable In the pre-harvest environment, many pathogens. Developing economies rep-
impact on microbial populations. of the significant issues in microbiological resent major sources of certain im-


Thus, regular consumption of foods acid-sensitive enteric pathogens, wheth- 100 years ago (Metchnikoff, 1908).
containing probiotics has a strong po- er the pathogens are indigenous to the More recent examples include Saavedra
tential to help maintain a beneficial and intestinal population or opportunistic et al. (1994), who showed that supple-
stable intestinal microflora that pro- contaminants of food and water (Lang- menting infant formula with Bifidobac-
motes intestinal health. This is especial- hendries et al., 1995). terium bifidum and Streptococcus ther-
ly true for those subpopulations with A similar case for administration of mophilus can reduce the incidence of
compromised or underdeveloped gut probiotic cultures would be for the new- acute diarrhea and rotavirus shedding
flora, such as the elderly, infants, and born (Mitsuoka, 1989). Within a day of in infants; Bernet et al. (1994), who
patients treated with antibiotics or che- birth, bacteria commence colonization found that consumption of a greater
motherapy. For example, in the elderly, and proliferation in the previously sterile number of lactobacilli provided in-
there is a steady decline in numbers of intestinal tract. Initially, coliforms, en- creased protection against cell associa-
bifidobacteria and an increase in the terococci, staphylococci, and clostridia tion by enterotoxigenic and entero-
numbers of C. perfringens with age. appear, but in three to four days after pathogenic E. coli and S. Typhimurium,
With this shift in gut flora, there is a birth, lactobacilli and bifidobacteria pre- and against cell invasion by entero-
corresponding increase in putrefactive dominate. Bifidobacteria soon dominate pathogenic E. coli, S. Typhimurium and
substances in the intestinal tract that are all other bacteria, whether the infant is Y. pseudotuberculosis; and Okamura et
inherently toxic and impose a constant breast-fed or bottle-fed. However, in bot- al. (1986), who used a tissue culture in-
stress upon the liver (Mitsuoka, 1990). tle-fed infants, populations of coliforms fection assay to demonstrate that ad-
In addition to C. perfringens, the putre- and enterococci are ten times higher than ministration of Bifidobacterium infantis
factive organisms that convert amino in breast-fed infants, a fact that may en- prohibited invasion and intracellular
acids into amines and other toxic sub- courage the use of infant formula that multiplication of S. flexneri. In all, pro-
stances include Salmonella, Shigella, and includes probiotic cultures. biotic cultures have demonstrated an
E. coli. As a means to ameliorate these The feeding of probiotic cultures to inhibitive or antagonistic effect against
detrimental conditions, elevated levels prevent or treat disease is well estab- almost all foodborne pathogens, includ-
of bifidobacteria and lactobacilli from lished in the scientific literature. Elie ing Salmonella, Shigella, E. coli, Campy-
dietary probiotics reduce fecal pH to Metchnikoff of the Pasteur Institute first lobacter, Clostridium, Yersinia, Vibrio
discourage growth and colonization by promoted the use of probiotics nearly and Candida (Fuller, 1992).

Microbial Ecology and Foodborne Disease

The complexity of the pre-harvest, Improved understanding of these food safety are broad concerns that apply
harvest, and post-harvest environ- complex factors provides insight into to many different commodities. Because
these issues affect so many commodities,
ments makes it impossible to control pathogen evolution and opens the door improvements in these areas would have
all potential sources of microbial to new and improved prevention and significant food safety impact.
contamination. Efforts at prevention control methods.
and control are implemented through-
Global Food Trade
out the food production and processing Globalization of the world’s food
PRE-HARVEST ENVIRONMENT supply has contributed to changing pat-
system. Researchers are continually
terns of food consumption and food-
searching for a better understanding of Efforts to minimize microbial con- borne illness. A growing percentage of
the pathogens and their interaction tamination of food begin in the pre-har- the U.S. food supply is imported. The
vest environment. Raw ingredients are sheer volume of these imports adds to
with the environment, leading to one way in which pathogens are intro- the complexity of foodborne illnesses.
improved control technologies. But at duced into the processing environment. Global sourcing provides economic
the same time, the pathogens continue Unfortunately, pathogen control in the benefits and a wider selection for con-
production agriculture environment is sumers that improves nutrition world-
to evolve, and human actions some- often difficult. wide. However, in terms of disease
times drive that evolution. Even small control programs, globalization mini-
environmental changes can have Overarching Issues mizes traditional geographic barriers
to emerging as well as traditional
unforeseen or even unforeseeable In the pre-harvest environment, many pathogens. Developing economies rep-
impact on microbial populations. of the significant issues in microbiological resent major sources of certain im-


Table 8. Sources of Imported Fresh and Manure side the home; eating raw seafood; drink-
Frozen Produce (1997 data) (GAO, 1999) ing raw milk; living on or visiting a farm;
The widespread occurrence and use and having contact with farm animals or
Percent of animal manure as fertilizer is a grow- puppies (Friedman et al., 2000). Fecal
Country (by $ value) ing environmental concern, because it contamination is a common source of C.
contaminates: water for drinking, irriga- jejuni contamination for each risk factor.
Mexico 51
tion, aquaculture and recreation; the For example, poultry feces frequently
Canada 15 hides, coats, and feathers of farm ani- contain C. jejuni at populations of 105 to
mals; and farm equipment and build- 107 colony forming units of bacteria per
Chile 12
ings. In the United States, cattle, hogs, gram (CFU/g), resulting in levels of
Costa Rica 4 chickens and turkeys produce an esti- greater than 103 CFU C. jejuni per gram
mated 1.36 billion tons of manure annu- of carcass in 60 to 90% of retail poultry.
Netherlands 3 ally (EPA, 2000), with greater than 90% E. coli O157:H7 causes an estimated
Guatemala 2 attributed to cattle. Each year livestock 73,500 cases of infection in the United
create an estimated five tons of animal States annually. Its principal vehicles of
Other 13 manure per person living in the United transmission are beef, produce, water
States, meaning the amount of animal (both drinking and recreational), and
manure is 130 times greater than the contact with cattle (Doyle et al., 1997;
ports (see Table 8). For many of these amount of human waste produced (U.S. Griffin, 1998). Because E. coli O157:H7 is
countries, infectious diseases still rep- Senate Agriculture Committee Demo- carried in the intestinal tract of cattle, the
resent a significant burden of illness. cratic Staff, 1998). pathogen’s most frequent origin is direct
Diarrhea remains among the ten lead- Many of the most prominent food- or indirect contact with cow manure. Ma-
ing causes of death and disease burden borne pathogens in the United States, in- nure can contaminate food when used as
in the developing world (Murray and cluding Campylobacter jejuni, Salmonella a soil fertilizer, when it pollutes irrigation
Lopez, 2001). and Escherichia coli O157:H7, are carried water, when cattle defecate near produce
Imported foods can introduce patho- by livestock and are principally transmit- or foods of animal origin, and when in-
gens previously uncommon in the United ted to foods by fecal contamination. C. testinal contents or manure-laden hides
States, such as Cyclospora and new strains jejuni accounts for an estimated 2 mil- contact carcasses during slaughter and
of Salmonella. Raspberries from Guate- lion cases of foodborne illness annually, processing. Case-control studies of pa-
mala, cantaloupes and scallions from with poultry and unpasteurized milk as tients with E. coli O157:H7 infections re-
Central American countries, coconut milk its principal vehicles (Mead et al., 1999). vealed several major risk factors for ill-
from Southeast Asia, and a Middle East- Salmonella causes an estimated 1.3 mil- ness: eating undercooked ground beef, liv-
ern snack food have all been implicated in lion cases of foodborne illnesses annual- ing on or visiting a farm, and having con-
recent foodborne disease outbreaks in the ly, with eggs, poultry, beef, pork and pro- tact with farm animals, especially cattle
United States. As the percentage of im- duce as primary vehicles (Mead et al., (Kassenborg et al., 1998). Depending on
ported foods consumed in the United 1999). Both C. jejuni and Salmonella are environmental conditions, E. coli
States increases, the importance of ensur- carried in the intestinal tract of appar- O157:H7 can survive in manure for many
ing that these foods are safe increases as ently healthy poultry and livestock. Fecal weeks, and in some instances for more
well. Food safety therefore cannot be contamination of hides, feathers and than one year. Similarly, the pathogen can
achieved by focusing on domestic prod- skin occurs during poultry and livestock survive well in lake water, with as little as a
ucts exclusively (GAO, 1998). production and slaughter. This contami- 10- to 100-fold reduction occurring dur-
As shown in Table 9, the import nation can subsequently carry through ing 13 weeks at 8 C.
share of some commonly consumed to processing. A case-control study of Increased proximity and animal den-
foods is increasing. For example, in patients with Campylobacter infection sity during production contribute to
1995, one-third of all fresh fruits identified the following risk factors for problems of pathogens in runoff water
consumed in the United States was campylobacteriosis: foreign travel; eat- because the difficulty of manure man-
imported, and this trend is likely to ing undercooked poultry; eating chicken, agement is increased with greater vol-
continue. turkey or non-poultry meat cooked out- ume. Another issue is composting of ma-
nure by farmers, including organic farm-
ers. The conditions that effectively de-
Table 9. Percentage of Total U.S. Consumption Provided by Imports (GAO, 1998) stroy pathogens are not well defined.
Also, manure handling in other coun-
% Change
tries may be worse than in the United
Import Item 1980 1985 1990 (1980-95)
States, a serious concern for imported
Fish & shellfish 45.3 53.8 56.3 55.3 22.1 foods. Human feces from field workers
without access to adequate sanitation fa-
Fresh fruits 24.2 28.0 30.7 33.3 37.6
cilities remains an issue as well.
Fresh vegetables 7.6 8.9 8.4 11.7 53.9
Tomatoes for processing 1.4 7.0 5.7 3.5 150.0 Water
Broccoli for processing 9.1 22.2 57.8 84.9 833.0 In the pre-harvest environment, wa-
ter can be obtained from a variety of

sources, although ground water and well animal fecal material may contain a wide more complex. Complicating the situa-
water are perhaps the most widely used. variety of potential human pathogens, it tion further, microorganisms rapidly
Most farms do not provide specific treat- appears that the heartier survivors, such adapt to new, adverse environmental
ment of water for use in agricultural as parasitic protozoan oocysts conditions, allowing them to survive and
production, and the water sources rou- (Cryptosporidium spp.) are likely to pose replicate under extreme conditions in-
tinely used in agriculture can become the greatest risk (Beuchat, 1996; Jaykus, volving high and low temperatures, pH,
contaminated by a number of means. 1997). Also, the relative importance of osmotic pressures, and oxygen levels that
Perhaps the most common source is ani- contaminated irrigation water as op- are inhospitable to most higher forms of
mal manure contamination of runoff posed to direct fecal contact is unknown life (Jay, 2000; Kushner, 1980).
water; less common is contamination of for pathogens such as Campylobacter, As discussed in the previous section,
water with untreated human sewage, Listeria monocytogenes, E. coli O157:H7, American diets contain increasing
which is largely under control in the and Cyclospora cayetanensis. amounts of fresh fruits and vegetables.
United States and other developed coun- Produce is commonly consumed raw
tries, but of considerable concern for Typical Pre-Harvest Environment (unprocessed), which makes it impossi-
foods produced in developing countries for Foods of Plant Origin ble—with the currently available tech-
with inadequate water resources. Water nologies—to guarantee it is free of con-
sources also may become contaminated The microbiological status of a food taminating pathogenic microorganisms
by fecal excrement from wild animals or product at the time of consumption is a when consumed.
by general contamination of soil, but the function of its history. What kinds of mi- To control foodborne illness, the en-
significance of these to food safety is croorganisms and how many exist on tire food supply chain must be consid-
largely unknown. and in the food are a direct result of the ered (Baird-Parker, 2000). In the case of
Associations have been made be- circumstances of its production and Salmonella transmission (Baird-Parker,
tween the presence of pathogens in wa- handling. During the pre-harvest pro- 1990), direct contributing factors for the
tering troughs and their subsequent duction period and the harvest process, contamination of pre-harvest produce
prevalence in animals. For instance, in- many opportunities exist for microor- include contact with manure, water, hu-
vestigators have reported isolation of E. ganisms to contaminate food materials. mans, livestock, wildlife, pets, environ-
coli O157:H7 in water troughs sampled During the past 50 years, farming prac- mental pollution and effluent/sewage.
from cattle farms (Faith et al., 1996; Mid- tices have changed considerably. In gen- The primary source is considered to be
gley and Desmarchelier, 2001; Sargeant eral, intensive farming practices have im- contact with human or animal feces. As
et al., 2000; Shere et al., 1998), and others proved process control but also have noted above, water is a major concern
have reported that the practice of flush- contributed significantly to the rapid because it is used so extensively in farm-
ing alleyways with water to remove ma- spread of human and animal pathogens ing.
nure results in as much as 8-fold in- by creating more concentrated environ- Not all bacterial and fungal food
creases in animal carriage rates (Garber ments for pathogens to multiply and pathogens exist in the pre-harvest envi-
et al., 1999). Furthermore, the organism evolve and by generating larger quanti- ronment as a result of human or animal
is able to persist for days at ambient tem- ties of subsequently contaminated food fecal contamination. For example, many
perature in both soil and water (Maule, (Rangarajan et al., 2000). At the same sporeforming bacteria of food safety
2000; Rice and Johnson, 2000). Likewise, time, distribution networks have become consequence are native to soil and water,
it is recognized that contaminated water
is a significant source of Campylobacter
for infection of commercial poultry
flocks (Shane, 2000). Such contamina-
tion is usually followed by rapid, intra- Production Practices
flock dissemination, which has been ex- ing the 1990s, long-term climatic
acerbated by intensification of animal and Mycotoxins changes, or global warming from hu-
agricultural practices (Gibbens et al., A recent example of how changes man activities. The second causative
2001; Shane, 2000). in ecology and production practices factor is the increased use of no-till
Recent evidence of foodborne disease have affected mycotoxin incidence in agriculture methods, which have been
outbreaks associated with the consump- the United States is the massive in- implemented to reduce soil erosion.
tion of fresh produce has prompted crease in Fusarium head scab in Mid- Residual stubble left in a field during
some to consider the role of contaminat- western wheat and barley during the winter can provide a way for fusaria to
ed irrigation and surface runoff waters. last decade (McMullen et al., 1997). contaminate the following year’s crop.
Irrigation water containing raw or im- Head scab is often accompanied by el- As the environment changes,
properly treated human sewage can be evated contamination by deoxynivale- sometimes as a result of human ac-
the source of many pathogens, with Shi- nol (vomitoxin) and other trichoth- tion, the microbial populations adapt.
gella and the enteric viruses (hepatitis A ecenes. Two factors seem to have driv- Some environmental changes can in-
virus, Norwalk-like viruses, rotaviruses) en the head scab epidemic. One is an crease pathogen levels by providing
being perhaps the most significant increased spring rainfall during early favorable conditions; other changes
(Beuchat, 1996; Beuchat and Ryu, 1997). wheat head formation. The uncharac- can select for traits that result in resis-
Irrigation water contaminated with ani- teristic increase in rainfall may be a tant microorganisms that survive un-
mal fecal matter can also be a source of result of the prolonged El Niño dur- favorable conditions.
pathogens on fresh produce. Although


e.g., Clostridium botulinum and Bacillus able for treating invasive human infec- Salmonella (Threlfall et al., 1997). Al-
cereus. Mycotoxigenic varieties of fungi tions. though there is no evidence that the use
include Fusarium, Claviceps purpurea of antibiotics in feed is responsible for
and aflatoxin-producing strains of As- Use of Antibiotics the evolution of the multi-drug resistant
pergillus. In addition to known patho- strain of Salmonella Typhimurium
gens, the environment represents a sub- The widespread use of antibiotics in DT104, the rapid dissemination of this
stantial reservoir for potential emerging animal production and in the treatment strain in animals and humans indicates
pathogens. of human illness both facilitate the there is an advantage for strains with the
Because fresh produce undergoes emergence of antibiotic resistance. Mi- antibiotic-resistance phenotype (see
very little processing, emphasis at the croorganisms can develop resistance to sidebar, p. 44). S. Typhimurium DT104 is
farm level has been directed towards the antimicrobials through gene mutations the second leading cause of human sal-
prevention of microbial contamination or by acquiring transferable genetic ele- monellosis in England and Wales
rather than relying on corrective actions ments, such as plasmids and conjugative (Anonymous, 1996) and the most com-
once contamination has occurred. Al- transposons, that harbor resistance mon Salmonella species isolated from
though preventing contamination of genes. These mobile genetic elements cattle (Hollinger et al., 1998). S. Typh-
crops by pathogenic microorganisms is are important in horizontal transmis- imurium DT104 is resistant to ampicil-
important, it is very difficult to accom- sion of genes from the resident to tran- lin, chloramphenicol, streptomycin, sul-
plish consistently and reliably, given the sient microflora of the intestinal tract fonamides, and tetracycline (known as
large number of possible sources of (Levy et al., 1976). In addition to the R-type ACSSuT). The resistance genes to
pathogens prior to harvest. Science- mobility of the genetic elements, the an- the antibiotics are located on the chro-
based farming guidelines, known as tibiotic-resistant bacteria can be trans- mosome rather than a plasmid, indicat-
good agricultural practices, have been mitted to different animal hosts. A tet- ing they are nonmobile and stable
developed to control microbial contami- racycline-resistant E. coli strain from (Threlfall et al., 1995). In the United
nation in an effort to improve the safety cattle was traced to humans, mice, pigs, States, the ACSSuT resistant pattern was
of produce (FDA/CFSAN, 1998). and fowl found at the same location present in 28% of 976 S. Typhimurium
(Levy et al., 1976). The selective pressure isolates collected nationally in 1995, a
Typical Pre-Harvest Environment caused by antibiotic administration substantial increase from 7% in 1990
for Foods of Animal Origin causes the microbial populations that isolates (Hosek et al., 1997). Human in-
harbor the appropriate resistance fection by S. Typhimurium DT104 has
Meat animal production has in- determinant(s) to flourish (Levy, 1992). greater morbidity and mortality than the
creased dramatically since 1975 (USDA/ These antibiotic-resistant microbes can other nontyphoid Salmonella infections
NASS, 2000). The largest increase has make their way to humans through con- (Wall et al., 1994). Because the accumu-
been in poultry production, which rose taminated foods or animal-to-human lating data from molecular subtyping
from approximately 10 billion pounds in transmission (Angulo et al., 2000; methods and epidemiological investiga-
1975 to 40 billion pounds in 1999. Cattle Holmberg et al., 1984), although the tions suggest that the use of sub-thera-
production has remained relatively steady public health impact of the use of veteri- peutic levels of antibiotics in animal
since the early 1970s at approximately 41 nary drugs is difficult to measure (How- feeds plays a role in the emergence of an-
billion pounds. In addition to cattle and gate, 1997). tibiotic-resistant foodborne pathogens,
poultry, 24 billion pounds of pork are The contribution of sub-therapeutic the prudent and judicious use of antibi-
produced annually. These production levels of antibiotics in animal feed to the otics in both the agricultural and medi-
quantities, coupled with limited space for emergence of antibiotic-resistant patho- cal sectors is needed.
livestock on the farm, promote the dis- gens has been debated for years (Fein-
semination of microorganisms such as man, 1998). A growing body of evidence Feeding Practices
salmonellae. A higher prevalence of from epidemiological data and trace-
pathogens in food animals increases the back studies indicates that agricultural Another animal production practice
chances that meat will become contami- use of antibiotics plays an important with potential ramifications for microbi-
nated, providing a route for the pathogens role in the emergence of some antibiot- ological food safety is farm animal diet
to reach humans. Furthermore, to in- ic-resistant bacteria (Angulo et al., composition. A change of diet, for exam-
crease livestock health, feed efficiency, and 2000). A review of Salmonella out- ple, can change the microbial ecology of
growth rates in these confined conditions, breaks between 1971 and 1983 revealed the ruminant digestive system. Many
antibiotics are often added to animal feed, that antibiotic-resistant strains were studies have evaluated the effect of di-
potentially contributing to the develop- more likely to originate from animals etary changes on fecal shedding of E. coli
ment of antibiotic-resistance in microor- than were strains without resistance O157:H7 or acid-tolerant E. coli by cattle
ganisms that live in animals (zoonotic mi- (Holmberg et al., 1984). Additionally, or sheep, with conflicting results. Some
croorganisms) (Angulo et al., 2000; Witte, the emergence of Salmonella with de- investigators have determined that sheep
1998). Approximately half of the antimi- creased susceptibility to fluoroquino- or cattle fed hay shed E. coli O157:H7 in
crobials produced today are used in hu- lone paralleled approval of the veteri- their feces considerably longer than ani-
man medicine; most of the remainder is nary use of enrofloxacin, a fluoroqui- mals fed grain (Hovde et al., 1999; Kudva
added to animal feed (WHO, 2002). The nolone antibiotic, even though fluoro- et al., 1997). In contrast, studies of acid-
emergence of antibiotic-resistant human quinolones had been used in humans tolerant E. coli, which is a characteristic
pathogens like Salmonella and Campylo- for the preceding six years with little im- of E. coli O157:H7, revealed that a mostly
bacter spp. limit therapeutic options avail- pact on the development of resistant grain diet promotes shedding of acid-tol-

Development and
parent failure of treatment with ciproflox- (Cetinkaya et al., 2000).
Dissemination of icin. During the 1990s, an increased oc- The strains of S. Typhimurium
currence of resistant C. jejuni isolates in DT104 that became a global public
Resistant Organisms Minnesota was associated with treatment health concern during the 1990s ap-
Microorganisms develop resis- with a fluoroquinolone antibiotic and pear to be highly clonal (Baggeson et
tance to antibiotics encountered in foreign travel. However, a growing pro- al., 2000). Although DT104 appears to
clinical and environmental settings. portion of resistant isolates was not at- have accumulated multiple resistance
This fact has led to calls for the judi- tributable to these sources. Surveys of genes through horizontal gene trans-
cious use of antibiotics in human chicken at retail markets in Minnesota fer, these genes were likely accumulat-
medicine and for restrictions on the demonstrated a 20% prevalence of con- ed before the widespread dissemina-
use of antibiotics in veterinary medi- tamination with resistant C. jejuni strains. tion of the resistant strains. Wide-
cine and animal production. These strains showed considerable diver- spread dissemination of DT104 may
There are at least three fundamen- sity based on polymerase chain reaction have been facilitated by the use of an-
tally different ways that exposure to an- (PCR)-restriction fragment length poly- tibiotics on farms, either because indi-
tibiotics can promote the development morphism (RFLP) (PCR-RFLP) subtyp- vidual animals were treated with
and/or dissemination of resistant ing of the flaA gene, suggesting that muta- drugs that DT104 was resistant to, or
microorganisms: (1) mutations and se- tions and selection of mutants was inde- because use of antibiotics altered the
lection of mutants capable of surviving pendently occurring among many C. jeju- herds’ microflora and increased ani-
in vivo exposure to the antibiotic (e.g., ni strains. The overlap of molecular sub- mals’ susceptibility to colonization
fluoroquinolone resistance in C. jejuni), types obtained from human and chicken and infection (Besser et al., 2000).
(2) mobilization and horizontal trans- sources suggest that chicken was a prima- Although fluoroquinolone resis-
fer of genetic elements containing resis- ry source of resistant C. jejuni for humans tance in C. jejuni appears to be a direct
tance genes among different species of that were not treated and did not travel response to clinical or environmental
bacteria (e.g., vancomycin resistance (Smith et al., 1999). exposure to the antibiotics, DT104 rep-
among enterococci), and (3) wide- In Europe, a glycopeptide antibiotic, resents the epidemic spread of a micro-
spread dissemination of strains with avoparcin, was used as an antimicrobial organism that has already developed
previously developed resistance (e.g., S. growth promoter. Following its introduc- resistance. The origins and factors con-
Typhimurium DT 104). The differences tion, resistance of enterococci to vanco- tributing to the dissemination of these
between these mechanisms have impor- mycin (a similar glycopeptide antibiotic) organisms require public health mea-
tant implications for the prevention was observed in hospitalized patients, ex- sures that address the differences. Try-
and control of antibiotic resistance posed animals, and the human popula- ing to accomplish comprehensive con-
among foodborne bacteria. tion outside of hospitals. Vancomycin- trol of these different situations prima-
Resistance of C. jejuni to fluoroqui- resistance genes were transferred hori- rily through restrictions on the veteri-
nolones is conferred by a point muta- zontally between species of enterococci nary and agriculture use of antibiotics
tion in the gyr gene (Engberg et al., (Simonsen et al., 1998; van den Braak et has created an adversarial relationship
2001). Resistant organisms with the al., 1998). The potential for vancomycin- between public health and animal pro-
same molecular subtype characteristics resistance genes to be acquired by strains duction communities that has imped-
as sensitive microorganisms have been of Staphylococcus aureus represents an ed the application of science-based
isolated from human patients after ap- important public health threat control strategies.

erant E. coli in comparison to hay-fed fecal shedding of E. coli O157:H7 by cat- flora—in the gastrointestinal tract of an-
cattle (Diez-Gonzalez et al., 1998). Sub- tle (Buchko et al. 2000). Feces of cattle imals may be able to prevent coloniza-
sequent studies revealed that changing fed 85% barley were more frequently E. tion by pathogens (Nurmi and Rantala,
the diets of cattle from grain to hay or coli O157:H7-positive than those from 1973). In chickens for example, the gut
from hay to grain distinctly reduced fecal cattle fed 85% corn, although no major of the hatchling chick is sterile until it in-
shedding of Shiga toxin-producing E. coli differences were observed in cell num- gests microorganisms from the environ-
(STEC) within the first week after chang- bers of E. coli O157:H7 in feces through- ment. If the chicks are exposed to adult
ing the diet, whereas the E. coli cell num- out most of the study. Before specific bird fecal material, colonization of the
bers increased considerably thereafter diet and feeding practices can be practi- gut occurs rapidly. Today’s production
(Richter et al., 2000). Overall, a major cally applied to farm production practic- practices remove this route of coloniza-
change in the composition (i.e., grain or es for pathogen control, considerably tion, and the hatchling may not acquire a
roughage) of the ruminant diet appears more research is needed to elucidate the normal gut flora for days or weeks
to decrease for a few days the number of influences that different dietary practices (Spencer and Garcia, 1995). The lack of
STEC shed in feces. Thereafter, cell contribute to gastrointestinal carriage a fully developed “normal flora” increas-
numbers of the pathogen increase. and fecal shedding of pathogens. es the chances of the chick gut becoming
Recent evidence indicates that the As with humans, “good” bacteria—in a carrier for microorganisms, such as
type of grain fed to cattle can influence some cases nonpathogenic normal gut Salmonella, that are pathogenic in hu-


mans. The chicken is most susceptible to proximately 1% of all cases, and up to sewage. For a number of reasons, the fe-
colonization by human pathogens dur- 13.3% of food-related deaths are due to cal coliform index is inadequate for
ing the first week of life (Nurmi et al., the consumption of contaminated shell- monitoring the presence of viral contam-
1992). The prevention of colonization fish (Bean et al., 1997), although the to- ination in shellfish or their harvesting
with pathogens by normal gut flora is tal number of cases is likely to be un- waters, and both outbreaks and sporadic
called competitive exclusion. derestimated (Wallace et al., 1999). cases of enteric viral disease associated
The use of probiotics in animals has Two general groups of pathogenic mi- with the consumption of contaminated
expanded to include virtually all food croorganisms may be transmitted by fe- shellfish continue to occur in the United
and food-producing animals, as well as ral shellfish. The first group is termed States (Jaykus et al., 2001). Protozoan
companion animals. The concept is the indigenous pathogens because these or- parasites such as Giardia and Cryptospo-
same as for the human use of probiotics, ganisms are native to the marine envi- ridium species have recently been identi-
that is, maintaining a healthy gut flora ronment, consisting predominantly of fied in feral shellfish (Fayer et al., 1998),
enhances health and may prevent coloni- members of the family Vibrionaceae, in- although the significance of this food
zation with pathogens. Probiotics are cluding the genera Vibrio, Aeromonas with respect to disease transmission has
administered to maintain health under and Plesiomonas. The presence of these yet to be determined. Shellfish harvest-
the stresses animals experience due to organisms is unrelated to fecal pollu- ing beds become contaminated with par-
crowding, transportation, overwork, and tion. The second group, referred to as asitic protozoa as a result of contamina-
other external forces, and also to increase non-indigenous pathogens, are not nat- tion with animal farm runoff or human
feed efficiency. They are touted as possi- ural marine inhabitants, and their pres- sewage, both treated or untreated.
ble alternatives to antibiotics in some sit- ence in shellfish arises from either direct The indigenous bacterial pathogens
uations. Most probiotics used in ani- fecal contamination by human or ani- (most notably Vibrio cholerae, Vibrio
mals currently are single microorgan- mal reservoirs, or due to poor general parahaemolyticus, and Vibrio vulnificus)
isms or defined mixtures of microorgan- sanitation during harvesting, process- are part of the estuarine microflora and
isms. Current policy prevents unquanti- ing, or preparation of the food animals. have excellent survival capabilities in the
fied or unidentified (undefined mix- Within these two major groups, we can marine environment. In addition, V.
tures) of microorganisms to be used as further characterize microorganisms cholerae from human sewage may con-
“direct-fed microbial products” that can contaminating shellfish as bacterial, vi- taminate the marine environment. While
be regulated as food under Food and ral or parasitic protozoan in nature. the transmission of V. cholerae by sea-
Drug Administration (FDA) Compliance The presence of Salmonella and Shi- food is well documented throughout the
Policy Guide (CPG) 689.100 (FDA/ gella species in feral shellfish is well doc- world, the United States has not had a
CVM, 1997). Many competitive exclu- umented, even in the recent literature. major outbreak since 1911, although
sion products, particularly those that These organisms are an excellent exam- sporadic cases have occurred, usually
claim to exclude Salmonella, are regarded ple of non-indigenous bacterial patho- due to the consumption of imported
as drugs by FDA. gens, the presence of which is usually due crustacea such as crabs and shrimp
to fecal contamination of harvesting (Bean et al., 1997). Historically, V. para-
Wild-Caught Shellfish and Fish sites. Fortunately, the National Shellfish haemolyticus outbreaks are rare in the
Sanitation Program sponsors long-term United States, but two highly publicized
Feral shellfish present a unique op- programs targeting the prevention of recent outbreaks have challenged this
portunity to transmit foodborne diseases shellfish-associated disease caused pri- trend (CDC, 1998b; CDC, 1999b). Shell-
of bacterial, viral and protozoan origin. marily by enteric bacteria. In the United fish implicated in these outbreaks were
Of particular concern are the edible bi- States, this program has established bac- harvested from both Atlantic and Pacific
valve molluscs of the class Pelecypoda that teriological standards for shellfish and waters during these outbreaks, but in
include the species commonly referred to their harvesting waters based on the fecal both cases, the mean surface water tem-
as oysters, mussels, clams, and cockles. coliform index. Such standards have peratures were significantly higher (1-5
Since most of these organisms are filter been quite effective in preventing enteric C) than those reported in previous years.
feeders, they use siphoning organelles and bacterial contamination of feral shellfish, This phenomenon suggests the potential
mucous membranes to sieve suspended and with the exception of species im- for emergence of this pathogen is associ-
particles from the aquatic environment as ported into the United States from coun- ated with natural changes in the temper-
a source of food. If their surrounding wa- tries with less stringent standards, out- ature of the Gulf Stream (El Niño) or
ter is contaminated by bacteria, viruses, or breaks of shellfish-borne disease associ- global warming from human activities.
parasitic protozoa, these mucous mem- ated with Salmonella and Shigella are rel- V. vulnificus has been of greater con-
branes may entrap the pathogens, which atively uncommon in the United States. cern in the United States in recent years,
are then transferred to the digestive tract This is, however, not the case for the since this organism results in a syn-
of the animal. Since these molluscan non-indigenous viral and protozoan drome characterized by gastrointestinal
shellfish may be consumed whole and pathogens that may be transmitted by disease followed by primary septicemia,
raw, they can act as passive carriers of hu- contaminated shellfish. Enteric viruses, with mortality rates approaching 50%.
man pathogens. most notably hepatitis A virus and the Individuals with underlying liver dys-
The most recent Centers for Disease Norwalk-like viruses (NLVs) are excreted function, circulatory problems particu-
Control and Prevention (CDC) statistics in the fecal matter of infected persons larly related to diabetes, or those who are
(1988-1992) of the overall foodborne and hence their source in the marine en- immunocompromised are especially at
disease burden in the United States esti- vironment is usually the disposal of un- risk (Hlady and Klontz, 1996). Evidence
mate that 0.7-2.1% of all outbreaks, ap- treated or inadequately treated human exists that other Vibrio species also can

The Role of Microbio-
the presence of pathogens (Banks and ings as indicators of enteric pathogens.
logical Indicators in Board, 1983). Ideally, the absence or a The relationship between the pres-
low concentration of a specific indicator ence of the fecal indicators and the
Assuring Food Safety means the food has not been exposed to presence of foodborne pathogens of
The term “microbiological indica- conditions that would permit contami- fecal origin, such as Salmonella and
tor” refers to a microorganism, a nation by a specific target pathogen or Campylobacter, has been questioned
group of microorganisms, or a meta- present the opportunity for its growth. for years. Recently, Kornacki and
bolic product of a microorganism, The indicator concept can be used to Johnson (2001) stated that “numerous
whose presence in a food or the envi- evaluate raw product directly from the studies have determined that E. coli,
ronment at a given level is indicative of field or farm, or after some decontami- coliforms, fecal coliforms and Entero-
a potential quality or safety problem. nation or inactivation process. bacteriacae are unreliable when used
The selection of an appropriate indica- Selection of an indicator that is rele- as an index of pathogen contamina-
tor is highly dependent upon the mi- vant for a given food and a given target tion of foods.” This unreliability ap-
crobiological criteria for the food pathogen continues to be a challenge. Be- plies to fresh produce (Anonymous
product in question. Important con- cause no microbiological indicator is ide- 2000; DeRoever, 1998; Nguyen-the
siderations in indicator selection in- al, food safety professionals are frequently and Carlin, 2000), fresh meats
clude: possible sources of pathogenic left with a limited choice of indicators that (Goepfert, 1976; Linton et al., 1976;
microorganisms; their incidence on or are relevant to some, but not all, food- Roberts, 1976; Tompkin, 1983), and
in the product; production, harvesting borne pathogens. The most widely used feral shellfish (Jaykus et al., 2001). In-
and processing practices; survival and indicators are the Enterobacteriaceae, dicators for other pathogens such as L.
growth of pathogens in the product; coliforms, “fecal” coliforms and E. coli. monocytogenes have perhaps fared bet-
and specific analytical methods avail- Coliforms are gram-negative asporoge- ter, and many processors continue to
able for detecting the indicator. nous rod-shaped bacteria that are envi- use the absence of generic listeria as an
Although frequently used inter- ronmentally ubiquitous and may be asso- indicator for the absence of L. monocy-
changeably, scientists sometimes make ciated with the fecal material of animals togenes.
a distinction between the terms micro- including humans. Coliforms are fre- Despite the clear need for more re-
biological indicator and index organ- quently used as an indicator of inade- liable indicator systems, all the candi-
ism. In general, index organisms are quate sanitation and process control in date replacements, such as coliphage,
markers whose presence in numbers food that receives a pasteurization heat Bifidobacter spp., and enterococci, have
exceeding pre-established limits indi- treatment. Among the proposed or ac- their own limitations. Beyond the
cates the possible occurrence of eco- cepted uses of E. coli are as an indicator of pathogenic bacteria, indicators also are
logically similar pathogens (Mossel et fecal contamination, acceptably condi- needed that are specific for human en-
al., 1995). Indicator tests are often em- tioned manure, acceptable quality of wa- teric viruses such as human calicivi-
ployed to assess a process control at- ter for irrigation, shellfish safety and gen- ruses (Norwalk-like viruses) and par-
tribute, such as using the extent of me- eral environmental sampling. Some orga- asitic protozoa such as Cryptosporidi-
sophilic growth as an indicator of in- nizations have used the entire Enterobac- um, Cyclospora, and Giardia, all of
adequate refrigeration (Ingram, 1977). teriaceae family as an indicator or index which tend to be more resistant and
A given marker can function both as of potential pathogen contamination. persistent than bacterial foodborne
an index and as an indicator organ- Other alternative indicators have included pathogens. As in so many other areas
ism, even in the same food. the coliphage group and the “fecal strepto- of food microbiology, additional work
The presence of indicator organ- cocci” or enterococci. Each of these in the area of microbiological indica-
isms does not necessarily guarantee groups of microorganisms has shortcom- tors remains essential.

result in septic disease, including V. para- that routine examination by conventional the fecal coliforms and important hu-
haemolyticus, V. cholerae non-O1, and cultural methods may provide negative man pathogens such as enteric viruses,
Vibrio hollisae (Hlady et al., 1993), a find- results although viable and potentially the pathogenic vibrios, and perhaps the
ing that may indicate the emergence of virulent cells may be present in high parasitic protozoa. In addition, shellfish
non-vulnificus Vibrio species as sources numbers (Oliver and Wanucha, 1989). harvested from other countries with less
of life-threatening shellfish-borne disease. Because regulation of seafood occurs stringent standards than those of the
V. vulnificus is a leading cause of food- predominantly by pre-harvest monitor- United States may be contaminated, and
borne disease-related deaths, particularly ing of the fecal coliform index of grow- some countries have much higher do-
in the southern states (Bean et al., 1997; ing waters, the efficacy of control is high- mestic rates of shellfish-associated dis-
Hlady et al., 1993). There is indication ly dependent upon the relationship be- ease. Pre-harvest control methods such
that the microorganism is capable of es- tween this test and the presence of patho- as relaying (movement of shellfish from
tablishing the so-called viable-but-non- gens. A significant relationship does not one harvest site to an alternative, pristine
culturable (VBNC) state, which means exist in shellfish between the presence of site to allow the animals to purge them-


selves of pathogens prior to harvest) have ents may be labeled as “made with organic aquaculture or commercial fish farm-
been effective for the elimination of ingredients” but cannot carry the USDA ing. To meet the demand for seafood
many of the non-indigenous bacterial seal. Although the available data do not products, the seafood industry is turn-
pathogens, but are reasonably ineffective indicate that organic foods are safer or ing to aquaculture to supplement in-
in controlling viral and Vibrio contami- more nutritious than conventional food, creasingly limited natural supplies. The
nation. In short, there is a need to fur- consumer surveys indicate that foods la- Food and Agriculture Organization
ther evaluate pre-harvest issues that im- beled with the USDA organic seal are per- (FAO) of the United Nations defines
pact the safety of feral shellfish con- ceived as being more healthful. aquaculture as the “farming of aquatic
sumed by the U.S. population. A significant public health concern that organisms, including fish, molluscs,
has been largely overlooked by the organic crustaceans and aquatic plants” (FAO,
Specific Production Methods movement is the potential for greater prev- 1995).
alence of contamination by foodborne The available data (primarily from
Sometimes the method used to pro- pathogens that are carried by livestock and temperate zones) indicate a low inci-
duce the food commodity has a signifi- poultry and shed in their feces. Manure, a dence of enteric pathogens in fish and
cant effect on the microbiological safety of significant vehicle for pathogens, is a major crustaceans raised in unfertilized sys-
foods. Organic foods are of special inter- source of fertilizer used for growing organ- tems, and few reports of human illness
est, in part because this production meth- ic produce. The available scientific infor- associated with the consumption of
od relies on manure as a major source of mation is insufficient to ensure that food- aquacultured finfish and crustaceans
fertilizer. In addition, aquaculture meth- borne pathogens are killed during com- (Jensen and Greenless, 1997). Howgate
ods have some significant food safety dif- posting and soil application. (1997) reported that there was no reason
ferences from traditional fishing. Furthermore, manure contaminates to expect the risk of illness from farmed
hides, feathers and skin during livestock marine fish to be greater than corre-
Organically Grown Foods production. During slaughter and pro- sponding wild species. In fact, the most
cessing, carcasses occasionally come in challenging public health risks from
Organic foods are the product of a contact with manure and become con- aquaculture are those associated with
farming system that avoids the use of taminated with pathogens. Because or- shellfish grown in open surface waters
manmade fertilizers, pesticides, growth ganic production standards prohibit the (Jensen and Greenless 1997), where
regulators, and livestock feed additives. In- use of irradiation and chemical treat- aquaculture faces many of the same is-
stead, the system relies on crop rotation, ments during processing, the available sues as wild caught.
animal and plant manures, some hand methods to reduce pathogen contamina- Antibiotics are used in aquaculture
weeding, and biological pest control. The tion are restricted, resulting in a greater to control disease in cultured species.
organic food industry has been growing likelihood that organic meat and poultry Drug use is regulated by FDA, but the
at an annual rate of 20 percent during the will have higher levels of pathogen con- number of approved drugs is limited and
past decade, and continued growth is pro- tamination than conventionally pro- off-label use has been reported (JSA,
jected. Produce grown by about 12,000 cessed meat and poultry. 1994). These antibiotic compounds are
organic farmers nationwide grossed ap- Very few studies have been conduct- allowed only for certain species and life
proximately $6 billion in 2000. The surg- ed to address the microbiological safety stages, with designated withdrawal peri-
ing market for organic produce is in part of organic foods. A relatively small study ods, during which cultured fish and
attributed to some consumers’ belief that was done to determine the prevalence of shellfish that have been treated with vet-
such foods are healthier, better tasting, E. coli and Salmonella on selected organ- erinary drugs cannot be harvested or
and produced using environmentally ic and conventionally produced vegeta- sold (JSA, 1994). Nevertheless, bacteria
friendly methods. Many consumers who bles available at Atlanta grocery stores resistant to antimicrobials have been iso-
have concerns about pesticides and herbi- (Doyle, 2000). A total of 216 samples— lated in farmed catfish and from their
cides cite safety as the main reason for use half organic and half conventional—was environment (DePaola et al., 1988), in
of organic foods. tested over a 6-week period. E. coli was sediments located beneath net pens (Ker-
In December 2000, the U.S. Depart- present on 22 organic samples and 18 ry et al., 1994), and from the intestines of
ment of Agriculture adopted marketing conventional vegetables, and Salmonella cultured fish in net pens (Ervik et al.,
standards for the processing and labeling was found in 3 organic samples and 2 1994). A World Health Organization re-
of organic foods (USDA/AMS, 2000). conventional vegetables. These data in- port on food safety issues associated with
The new standards do not allow the use of dicate that the organic produce sampled aquaculture products stated that the risk
irradiation, genetic engineering, and hu- was not safer from a microbiological to public health is probably limited to in-
man sewage sludge fertilizer for any food perspective than the conventional pro- direct exposure to antimicrobials (WHO,
labeled as organic. In addition, synthetic duce. A comprehensive survey of food- 1999). However, the use and misuse of
pesticides and fertilizers cannot be used borne pathogens in organic foods (in- antibiotics to control diseases in aquac-
for growing organic food, and antibiotics cluding produce, meats and poultry) is ulture is worldwide and will likely in-
and hormones are prohibited in livestock needed to more fully evaluate the relative crease as intensive aquaculture systems
production. Furthermore, livestock agri- microbiological safety of such foods. become more common.
cultural feed products must be 100 per- Current shellfish management pro-
cent organic. Products meeting the re- Aquaculture grams—which include classification and
quirements for labeling as “organic” can monitoring of growing waters, proper
carry a USDA Organic Seal. Products with One area where food production siting of aquaculture areas, enforcement
a smaller percentage of organic ingredi- has undergone dramatic change is of best management practices and train-

ing of employees and harvesters in sani- among workers. sites. Temperature control contributes
tation procedures—can help to reduce, An interesting practice in recent most to the safety of fruits and vegeta-
but do not eliminate, microbiological years has been the production of fresh- bles that are cut; however, its effective-
food safety issues. cut produce in the field. Presumably ness in controlling microbiological haz-
done to maintain product freshness, this ards is in general less significant than
practice essentially brings food process- the hazard reduction that occurs by re-
HARVEST ENVIRONMENT ing into the harvest environment. For ex- frigerating raw foods of animal origin
ample, many fresh-cut processors are (IFT, 2002).
The harvest environment is relatively now removing the outer leaves and cor-
commodity specific, because the meth- ing lettuce in the field. Some are even Food Animals
ods used and harvest locations depend cutting lettuce where it is grown. Unfor-
on the commodity in question. The har- tunately, it is much more difficult to con- Production livestock are naturally
vest environment is especially important trol contamination in the harvest envi- contaminated with a variety of potential
for foods such as fruits and vegetables ronment, and this practice may increase human pathogens, both externally and
that undergo minimal additional pro- the chances for contamination of these internally. These microorganisms origi-
cessing prior to consumption. products. Certainly contamination of nate from the environment in which the
wash and rinse water would be of con- animals are produced, as well as from
Produce cern under these circumstances, as feedstuffs and the co-mingling of ani-
would be issues associated with poor hy- mals from various sources. The animals
Many different approaches are used giene of food handlers and inadequate also can readily transmit these microor-
today to harvest produce depending on a sanitation of equipment. ganisms among themselves, once they
variety of determinants, including the Fruits and vegetables frequently are moved from the production environ-
type of produce, site of growing opera- come into contact with harvesting ment to the transportation system. Be-
tion, and labor availability. However, equipment (such as knives, machetes, cause of centralized slaughter establish-
from a microbiological safety perspec- clippers and scissors) and containers ments, production livestock may be
tive, there are many common hazards for (such as bins, boxes, buckets, pans, transported considerable distances be-
harvest operations. Water quality, field trailers, and truck beds). Such equip- fore slaughter.
worker hygiene, field sanitation, truck ment and containers should be properly During transportation, livestock are
sanitation, and temperature control are washed and disinfected, although stud- confined to prevent excessive move-
all food safety issues related to the har- ies indicate that washing and sanitizing ment. As the animals are in close physi-
vest environment (IFT, 2002). is done only about 75% and 30% of the cal contact, microorganisms may be
Water as ice or in the liquid form can time, respectively (USDA/NASS, 2001). transferred from one animal to another
readily transmit microorganisms to pro- Packing equipment such as tables, con- either by contact with each other or
duce if contaminated. Most fruits and veyor belts, flumes, and washing and their excreta. Aerosol transmission of
vegetables are washed with water at least cooling bins are washed and sanitized salmonella also has been demonstrated
once, and many types of produce are about 75% and 50% of the time, respec- in chickens and mice (Clemmer et al.,
treated with water several times during tively. 1960; Darlow et al., 1961). The upper
processing. In addition to being used for Equipment and containers used dur- respiratory tract may be important in
washing, water is used for cooling, con- ing harvest operations are frequently transmission, and the tonsils and lungs
veying produce (flume water), and for made of materials, such as wood, that are may be important sites for the invasion
applying disinfectants and fungicides. difficult to clean. Soil from the field, and dissemination of Salmonella in pigs
Disinfectants are added to about 50% to which may contain pathogens, often en- (Fedorka-Cray et al., 1995; Fedorka-
60% of water used in packing facilities. crusts equipment and containers. If not Cray et al., 2000; Gray et al., 1996).
Care must be taken to control the sani- removed, soil adhering to equipment Even under the best of conditions,
tary quality of water. used for washing and disinfecting pro- transportation produces measurable
Field worker hygiene is a major con- duce will reduce the sanitizing capacity stress upon live animals. Transport
sideration because of the widespread use of the disinfectant. Produce operations stress may have several physiological ef-
of human hands in cutting or picking must prevent accumulation of soil on fects on the live animal that may ulti-
vegetables and fruits in fields or or- equipment and containers to enable ef- mately impact food safety. Transporta-
chards. Approximately 90% of farms fective disinfection of food contact sur- tion of animals may increase fecal shed-
that grow fruit or vegetables harvest pro- faces. ding of potential human pathogens, such
duce exclusively by hand (USDA/NASS, Proper temperature control of fruits as salmonella. This increase in shedding
2001). The amount of human hand con- and vegetables is critical for both safety can contaminate the trucks or trailers
tact that occurs during harvesting varies and quality purposes. Optimal temper- used for transportation, and potentially
depending on the type of produce. Mel- atures vary according to the commodi- increase the population of foodborne
ons are handled at most steps of the op- ty; however, the temperature range for pathogens in and on many of the ani-
eration, whereas apples receive consider- storing fruits and vegetables is usually mals within the truck or trailer.
ably less frequent contact. Vegetables quite narrow. Most pathogens, but not Once animals arrive at a slaughter
such as leaf lettuce may be harvested, all, are inhibited by the cool tempera- establishment, they may be unloaded
trimmed, sorted and bagged by hand. It tures at which produce is stored. In ad- into holding pens prior to slaughter, de-
is very difficult to uniformly enforce dition, cool temperatures tend to pro- pending on the animal species in ques-
proper hand washing and glove use long the survival of viruses and para- tion. Animals from several trucks or


trailers may be co-mingled in the same processed on board the fishing vessel, refrigeration. Each of these stresses has
pen, although there is considerable while on the east coast and in the Gulf an impact on the microbial population
variation between slaughter establish- of Mexico, crabs are usually brought in the food.
ments. Co-mingling increases the op- alive to shore for further processing.
portunity for the spread of potential Lobsters are brought alive to shore, and Food Animal Slaughter and Meat
human pathogens between animals shrimp are iced or frozen on board the Processing
from different sources, with the possible fishing vessel.
outcome of more animals becoming All fishery products, regardless of Although food animal slaughter
contaminated either externally or inter- whether they are wild harvested or cul- could be considered a harvest activity,
nally with these microorganisms. In ad- tured, can be contaminated with a vari- from a microbial ecology perspective, it
dition, these holding pens are difficult ety of human pathogens. Although there occurs in the post-harvest sector of the
to adequately clean and sanitize, and it is no reason to expect cultured species to food chain. Slaughter and meat process-
is not uncommon to detect potential be any more hazardous than wild caught ing take place in a carefully controlled
human pathogens in these pens after (Howgate, 1997), there may be differenc- processing atmosphere that is different
they have been cleaned and sanitized es depending on the harvest area or cul- from the traditional harvest environ-
(Davies and Wray, 1997; Gebreyes et al., ture method. For example, FDA recently ment. Because food animals are natural-
1999). As a result, populations of bacte- found a higher percentage of Salmonella ly contaminated with a variety of poten-
ria may remain in these pens and con- spp. on farm-raised shrimp (7%) com- tial pathogens, meat processors apply
taminate animals that are brought in pared with wild-harvested shrimp (<1%) many microbiological control methods
from other sources. The same is true of (FDA, 2001). Most of the shrimp con- during the slaughter and processing of
poultry crates, which are equally diffi- sumed in the United States are imported meat.
cult to clean and sanitize. (NMFS, 2000), and a high percentage of
these shrimp are aquacultured in tropi-
Role of Inspection
Aquaculture and Wild-Caught cal countries. Reilly et al. (1992) reported
Fish and Shellfish that Salmonella spp. is a component of An important aspect of meat in-
the natural flora of pond cultured spection in the United States and other
The length of time between harvest shrimp in tropical countries. This find- developed countries is antemortem in-
and refrigeration is critical to the micro- ing may be due to the fact that in many spection. All animals presented for
biological safety of fish and shellfish. tropical countries, chicken manure is of- slaughter are inspected prior to slaugh-
Time/temperature abuse is of particular ten used as a fertilizer in aquaculture ter. At present, this inspection focuses
concern for the pathogenic Vibrio spe- ponds. To address food safety issues, on observable clinical illness, and not
cies. Rapid harvesting, cooling and pro- FDA is currently developing GAP guid- on general hygiene of the animals.
cessing influences quality, but it may ance documents to help reduce patho- However, because of the recognition of
also improve food safety for certain fish- gens associated with cultured fishery the impact of animal hygiene on meat
ery products by slowing the growth of products. contamination, there have been some
pathogens and reducing the formation attempts to regulate this on the live ani-
of histamine that causes scombroid poi- mal. For example, part of the antemor-
soning in certain species. POST-HARVEST ENVIRONMENT tem inspection in the United Kingdom
Commercial finfish are harvested by is an evaluation of the overall hygiene
a variety of methods. Fishing vessels may In the post-harvest environment, of the animal, and the animals may be
transport their harvests back to shore for food safety becomes less commodity ori- rejected for slaughter if they are too
processing on a daily basis, or they may ented, as the food moves through pro- “dirty.” Efforts to reduce the level of ex-
remain at sea for several days, weeks or cessing into the distribution and retail ternal carcass contamination of live ani-
even longer. Fishing vessels use several sectors. Microbiological food safety is- mals have typically focused on either
methods to preserve their catch (e.g., ic- sues in the processing environment have washing the entire animal or trimming
ing, freezing, or refrigerated seawater). the potential to affect many different the hair from the most heavily contami-
Finfish can be minimally processed on foods. Also, at the processing stage, in- nated areas of the animal (typically the
board (e.g., whole or eviscerated form). gredients from many different commodi- rump and midline of a steer or cow).
Finfish also can be processed into fillets ty sectors may be combined into a single These procedures must be balanced
and steaks and other value-added prod- product. As ingredients are combined, with animal welfare issues, which pre-
ucts, such as surimi (a washed, minced the physical characteristics of the food vent the introduction of excessive, need-
fish product) on commercial factory change, and its microbiological profile is less or unnecessary stresses on live ani-
ships. altered. mals.
Shellfish also may be processed on The microbiological controls ap-
board, or they may be brought to shore plied in the post-harvest environment
Source of Contamination
live. Mussels, clams, and oysters are are often designed to intentionally stress
usually quickly transported shore side the microorganisms present in the food. Contamination of animal carcasses
and shucked or sold as live whole shell- These stresses may be designed to be le- during slaughtering procedures is unde-
stock. Scallops are usually processed on thal on their own or in combination. sirable but unavoidable in the conver-
board the fishing vessel and stored iced Environmental conditions also may be sion of live animals to meat for con-
or frozen for several days or weeks. On modified to limit microbial growth, sumption. It is assumed that the muscle
the west coast, some crab species are through such techniques as drying or tissue of healthy animals entering the

slaughter establishment is free of micro- leaking bungs or an occasional rup- area of a carcass.
organisms (Ayres, 1955). However, in- tured gastrointestinal tract. In contrast to trimming, heat may
trinsic bacteria, occurring in the deep be applied as either a localized treat-
muscle tissue of healthy animals, have Impact of Interventions ment or as a whole carcass treatment.
been reported for many animal species The most common form of localized
(Ingram, 1964; Ingram and Dainty, Over the last twenty years, a number treatment currently in use is the steam
1971). The most frequently character- of interventions have evolved specifically vacuum. Steam vacuuming, as the name
ized intrinsic bacteria are Clostridium to address microbial contamination of implies, applies a steam treatment to
spp. (Canada and Strong, 1964; Jensen animal carcasses. These may be divided both loosen contamination and kill
and Hess, 1941; Narayan, 1966; Zagae- into physical methods and chemical bacteria, along with a vacuum process
vskii, 1973). Other potential human methods. In practice, these methods are to physically remove contamination.
pathogens, such as salmonella, have used in combination, resulting in a series Steam vacuuming may be highly effec-
not been reported as intrinsic bacteria of process interventions or “hurdles” to tive in reducing microbial populations
in the muscle tissue of healthy animals. improve the microbiological quality of under controlled conditions, but as with
The assumption is bacteria that con- meats. Among the physical methods, trimming, becomes less effective under
taminate the muscle tissue are from ex- prevention of contamination has re- processing conditions (Castillo et al.,
trinsic sources (gastrointestinal tract, ceived considerable attention. From the 1999; Dorsa et al, 1996). As an alterna-
lymph nodes, external carcass surfaces, perspective of microbial adaptation, it is tive to a localized treatment, heat may
and environmental sources). The ma- better to prevent contamination than to be applied as a whole carcass treatment.
jority of the microflora transferred to address it through processing methods. Common examples of this are singeing
the tissue surfaces, while aesthetically However, there are practical limitations of hog carcasses, hot water washing and
undesirable, is nonpathogenic. to this, given the nature of the process steam pasteurization. Heat in singeing
Carcass processing may be divided (i.e., converting a live animal to food for processes is commonly applied as open
into processes that impact the external human consumption). After prevention flame from gas jets, and while there is a
surfaces of the carcass and those that of contamination to the extent possible, reduction in microbial populations on
open the body cavity (evisceration). physical interventions involve either re- the carcass surface, the primary func-
Examples of surface processes include moval of contamination (trimming), tion of this process is to remove residual
the scalding of poultry and the remov- heat, or chemical treatments. hair from the carcass. In contrast, hot
al of beef carcass hides. These process- Effective physical removal of con- water washing and steam pasteurization
es in fact remove significant popula- tamination is dependent on first identi- were specifically developed as antimi-
tions of bacteria from the carcass, but fying the area of contamination and then crobial processes, applied as a final op-
also expose the edible tissue to con- removing the affected area without eration before chilling. Hot water wash-
tamination. While the process of hide transferring the contamination to other ing applies hot water (>80 C) as a whole
removal may be thought of as a prima- areas. There are practical limits to the carcass rinse, while steam pasteuriza-
ry source of contamination of beef car- identification of affected areas, as micro- tion places the carcasses in a chamber
casses, it also removes significant con- organisms cannot be seen. Therefore, and applies steam to briefly raise the
tamination from the carcass. In a simi- identification of an affected area requires temperature of the carcass surface.
lar fashion, scalding and de-feathering that there be sufficient contamination Both hot water and steam pasteuriza-
of chickens removes significant con- (mud, manure, etc.) to become visible to tion have been demonstrated to be ef-
tamination from the chicken carcass, the operator. Once the area has been fective in controlling microbial popula-
although some still remains on the car- identified, the operator must then re- tions on animal carcasses (Barkate et
cass. The microflora deposited by move the area in an aseptic manner. The al., 1993; Gill et al., 1995; Phebus et al.,
these processes is primarily from envi- probable outcome of this operation, un- 1997). However, surviving pathogens
ronmental sources, that which is on the der controlled conditions, is the complete will have undergone stress that may ei-
carcass from the livestock production removal of the contamination with a vir- ther increase or decrease the likelihood
environment and transportation. This tually sterile surface remaining around of their survival during the remaining
microflora may include enteric patho- the affected area. However, while this is time before consumption.
gens, such as salmonella and E. coli easily accomplished under controlled Chemical interventions involve the
O157:H7, and microorganisms such as conditions, it becomes much more un- application of food grade chemicals to
Listeria and Clostridium. From a mi- likely in a processing environment. The the carcass surfaces to inhibit or kill mi-
crobiological perspective, contamina- operator must clean and sanitize the croorganisms (Dickson and Anderson,
tion of edible tissue by external surface equipment (knife and hook) prior to the (1992; Siragusa, 1996). Typically, the
processing is a relatively common oc- operation, remove the affected area from mode of action of these antimicrobials is
currence. a carcass which is frequently moving on pH, with organic acids, such as lactic or
Processes that open the body cavity a processing line, and then re-sanitize the acetic (low pH) and trisodium phos-
expose edible tissue to bacteria from equipment prior to trimming the next phate (high pH), the most commonly
the gastrointestinal tract. The primary affected area. In practice, trimming is used. The concerns with the use of any
bacteria of potential public health con- substantially less effective in processing chemical intervention process are both
cern from this source are the enteric environments than in laboratory envi- the potential to induce resistance in po-
pathogens. In the case of red meat pro- ronments (compare Gorman et al. tential human pathogens and the poten-
cessing, this source of contamination is (1995) with Reagan et al. (1996)). Trim- tial to select for resistant organisms out
infrequent, and usually confined to ming as a process is limited to a specific of the overall microbial population. If re-


sistance becomes widespread in a micro- microbes. The common methods of car- objectives have been achieved in the
bial population, more organisms will cass chilling involve either forced air, slaughter process, and that the fabrication
survive, making the process less effective. forced air and water, or water chilling. process is maintained at a reasonable level
Perhaps the chemical intervention of While the primary intention of chilling is of hygiene, further interventions may be
greatest interest and concern is the or- to limit microbial growth, some chilling unnecessary.
ganic acids and their potential to induce methods do contribute to a reduction in
acid tolerance. In controlled experi- microflora. For example, forced air chill- Ground Meats
ments, acid-tolerant bacteria were no ing dries the carcass surface and may in-
more tolerant to organic acid rinse pro- jure or kill some microorganisms by de- Ground meats are a special category
cesses and were in general more sensitive hydration. The initial combination chill- of fresh meats. Ground meats are made
to heat than their homologous non-acid- ing process using forced air and water from the less desirable cuts of fresh meat
tolerant strains (Dickson and Kunduru, was the Chlor-Chil process (Swift and and from the trimmings of the more de-
1995). This suggests that the develop- Company, 1973), which used chilled sirable cuts of meats. Unlike a steak or a
ment of acid tolerance does not present a chlorinated water to simultaneously re- chicken breast, which originate from a
unique hazard with organic acid rinses duce microbial populations and chill the single carcass, ground meat may contain
on animal carcasses. carcasses more rapidly. Although the use meat from many different carcasses. The
Acid adaptation has been shown to of chlorine in the water is no longer nature of the process is to grind and mix
enhance the ability of salmonella to sur- widely practiced, the process now com- the meat, which increases the likelihood
vive in acidic food systems (Leyer and monly known as spray chilling is almost that a single contaminated carcass may
Johnson, 1992). These authors reported universally used in the beef industry. Al- contaminate a larger quantity of meat. An
that when salmonella were briefly ex- though it does not have the benefit of additional factor is that the trimmings
posed to mildly acidic conditions (pH drying the carcass, spray chilling reduces from the intact cuts of meat are often
5.8), the survival of these bacteria was the surface temperatures of carcasses from the surface of the cut. Because the
dramatically enhanced in cheese. Anoth- more rapidly than air chilling, and, since most consistent source of contamination
er study reported that S. Typhimurium virtually all of the bacteria are on the on animal carcasses are the processes
briefly exposed to mildly acidic condi- carcass surfaces, it effectively reduces mi- which affect the external surfaces of the
tions (pH 5.8) was significantly more re- crobial growth to a greater extent than carcass, the raw materials used for grind-
sistant to strong acid conditions (pH 3.3) air chilling. Water chilling, widely used in ing have a higher probability of being
than the non-adapted parent strain (Fos- the poultry industry, has evolved from a contaminated with bacteria of potential
ter and Hall, 1990). Acid shock at pH 4 significant source of contamination be- human health significance. A conse-
has also been reported to enhance the tween poultry carcasses to a potential quence of these factors is that the micro-
thermotolerance of L. monocytogenes microbial intervention process, with the bial populations in ground meat are con-
(Farber and Pagotto, 1992). Foster and use of counter-flow chillers and the addi- sistently higher than those on intact meat.
Hall (1990) reported that the adaptive tion of processing aids. Other than irradiation, there are essential-
acid tolerance response of S. Typhimuri- ly no commercially viable interventions
um did not appear to induce cross pro- Fabrication for raw ground meats at this time.
tection with hydrogen peroxide or heat A process that has also been used to
shock. Rowbury (1995) discussed the The disassembly of chilled carcasses is recover edible tissue from bones is me-
impact of a variety of environmental fac- referred to as fabrication. The outputs of chanical de-boning. This process was
tors on acid tolerance, and noted that or- fabrication are fresh meat to go to the first developed in the poultry industry,
ganisms attached to surfaces were more consumer, and meat intended for further but is also used in the red meat industry.
tolerant to acid than non-attached cells. processing. During fabrication, microor- Meat produced from mechanical de-
Buchanan et al. (1999) reported that pri- ganisms may be transferred from carcass boning processes resembles ground
or growth at acidic conditions increased surfaces to other parts of the carcass, and meat, but is used almost exclusively as a
the resistance of E. coli O157:H7 to ion- may be transferred from one carcass to processing ingredient for cooked meats.
izing radiation at acidic pHs. another by common contact surfaces. Be- This meat does not generally reach the
Acid-adapted microorganisms may cause of the latter phenomenon, one car- consumer as fresh meat. Because of the
have a competitive or ecological advantage cass has the potential to contaminate sev- nature of the process, mechanically de-
in the human stomach, which could po- eral other carcasses. As the fabrication boned meat commonly has a higher mi-
tentially impact pathogenicity. The theory process proceeds, the carcass identity is crobial population than other meats, in-
is that an acid resistant microorganism lost, and the potential for trace back is se- cluding ground meats.
would be more capable of surviving the riously diminished. Other than the physi-
acid pH of the stomach, and therefore cal intervention of preventing or reducing Processing
more organisms would enter the small in- contamination, there are essentially no
testine. This could then result in a lower commercially viable interventions in fab- Fresh meats are frequently further
infectious dose for the microorganism. rication at this time. This certainly pro- processed for specific flavor characteris-
vides opportunities for research and de- tics or for increased shelf life. The pro-
Chilling velopment, but it must be kept in mind cesses involved with meats are the pro-
that the objective of the slaughter opera- cesses commonly used with other foods,
Rapid chilling of hot (body tempera- tion is to place the least contaminated car- including thermal processing (cooking,
ture) animal carcasses is essential to re- cass into the chilling and fabrication pro- canning), dehydration, and fermenta-
duce the outgrowth of contaminating cesses. Assuming that the microbiological tion. These processes do not result in any

unusual microbiological hazards unique newly recognized food safety issues, into fillets and other value-added prod-
to meat products, but some of the com- such as E. coli O157:H7 in cattle and C. ucts. Fishery products may be consumed
mon microbiological hazards are worth jejuni in broilers, challenge the indus- raw, or they may be processed into
restating. try’s efforts. Continued improvements ready-to-eat products. Salmon, trout
Fermented meats, such as pepperoni, during slaughter may occur, but the bet- and other fish species are often processed
select for microorganisms that can toler- ter long-term strategy would be to min- into cold smoked and hot smoked fishery
ate higher osmotic pressure and acidic imize the presence of human pathogens products. Fishery products also are used
pHs. Microorganisms that can survive on the incoming live animals. This ap- in a variety of salads and spreads, and
and cause human health concerns in- proach would require changes in farm they are cured, fermented, pickled, dried,
clude S. aureus and some enteric bacte- management practices that are based on and canned. Rapid harvesting, cooling
ria, including E. coli O157:H7. Although scientific research. and processing can reduce or prevent
it is less likely that enteric bacteria will the occurrence of certain biological and
survive, cases of foodborne disease out- Post-Harvest Processing of Other chemical food safety hazards associated
breaks from these bacteria have been Commodities with some wild caught and cultured fish-
documented. ery species (e.g., molluscan shellfish and
Cooked, ready-to-eat meats are a Further processing of other com- scombrotoxin susceptible species) (NAS,
special category of processed meats. modities occurs as well. For example, 1991). In other instances, the use of food
These products undergo a thermal pro- fresh fruits and vegetables are frequently additives or other post processing inter-
cess that renders them fully cooked with sent to packinghouses where they may be ventions (e.g., high hydrostatic pressure,
a very low population of microorgan- washed, trimmed, or otherwise changed irradiation, or thermal pasteurization)
isms, and they are typically vacuum prior to packaging. The environment of may be required to control food safety
packaged and refrigerated. The refriger- the packinghouse, and anything that hazards.
ated shelf life of these products can reach comes into contact with the fresh pro- Regardless of the commodity, pro-
120 days, which provides an extended duce (e.g. water, conveyor lines, packag- cessing hazards can include pathogens
opportunity for psychrotrophic bacteria ing material) can thus contribute to the that may be naturally present on the
to grow. The specific human pathogen of microbial ecology of the produce, and food, that may be introduced during
concern is L. monocytogenes, which ac- can contaminate the produce with processing and handling, or that may in-
counts for approximately 30% of the pathogens. Since many fresh produce crease to hazardous levels during distri-
foodborne deaths in the United States items are ready-to-eat, the cleanliness of bution and storage. Strict attention to
(Mead et al., 1999). Because L. monocyto- the packinghouse environment is very good manufacturing practices, sanitation
genes in this case is a post-processing important. control procedures and hygienic practic-
contaminant, the intervention (heat) has Produce may be more extensively es of plant employees are effective in
already been applied, and there are few processed as “pre-cut” fresh fruits or veg- controlling many of these hazards.
intervention strategies that are viable af- etables. Pre-cut or shredded lettuce has
ter packaging. become a large industry serving the Water
A discussion of microbiological con- chain restaurant industry, as have other
trols in meat processing would not be pre-cut vegetables for salad bars. Pre- Water is used extensively in the post-
complete without considering the use of packaged salads are also a popular item harvest processing environment, making
irradiation (for detail, see irradiation, p. in grocery stores, and consumers fre- water quality a significant concern. Ad-
56). Irradiation has the advantage of be- quently believe no further washing is re- vances in water treatment over the last
ing able to penetrate packaging materi- quired when the items are brought into 100 years have resulted in dramatic im-
als. A product that is packaged and then the home for serving. Because the cut- provements to the microbiological safety
irradiated is protected from recontami- ting exposes more surface area and dis- of the public water supplies of developed
nation while the packaging material re- rupts natural barriers of the fruit or veg- countries (Dawson and Sartory, 2000).
mains intact. Irradiation may be the only etable, these items are more permissive of Perhaps of greatest present-day concern
effective microbial intervention process microbial growth. in these countries are large community-
for fresh products that, by definition, The seafood processing industry is wide waterborne outbreaks of parasitic
cannot be processed by conventional complex, and to maximize food safety, protozoa that are associated with either
processes. In a similar manner, irradia- processors and importers of seafood are unfiltered or inadequately flocculated or
tion may ultimately serve as an interven- subject to HACCP requirements as man- filtered water, such as the Cryptosporidi-
tion for packaged, processed meats. dated by FDA (FDA, 1995). The process- um outbreak that occurred in Milwaukee
ing of wild and aquacultured fishery in the early 1990s (MacKenzie et al.,
Future Challenges products can be as simple as washing 1994; Moe, 1996). It is important to note
molluscan and crustacean shellstock or that, although drinking water is quite
The net result of processing changes finfish with potable water. It also may safe in the United States, it remains a sig-
has been improved microbiological con- include shucking, filleting, beheading nificant cause of morbidity and mortali-
trol and reduced levels of enteric patho- and peeling followed by chilling and/or ty in developing countries, where water
gens. Since the adoption of these more freezing, for sale to wholesalers, distribu- remains a common source of bacteria,
comprehensive systems for pathogen tors and retailers. In some instances, fin- viruses, and parasitic protozoa that im-
control, the prevalence of salmonella fish, shellfish and crustaceans are sold pact human health. If this water is used
has decreased as determined by the live at the retail market, or processed by in food processing, waterborne diseases
USDA/FSIS monitoring program. But hand or machine at commercial facilities of developing countries can be passed on


to the consuming public in more devel- treatment facilities can be used on edible both the immediate impact and the po-
oped regions of the world through im- product only if the facility meets EPA re- tential ramifications further down the
portation of contaminated foods. quirements. Unfortunately, these facili- farm-to-table chain. Altering any param-
From the perspective of post-harvest ties are extremely expensive and most eter along the entire food chain can have
issues for produce, wash water, rinse wa- U.S. slaughter operations practice little if consequences beyond the immediate
ter, and ice can serve as a potential any routine water reuse at the current change, be they intended or unintended.
source for contamination of fresh pro- time. For example, modifying the feed of a
duce (Beuchat and Ryu, 1997). Perhaps food animal may alter the microbial con-
predictably, recent evidence suggests that Alternative Processing tamination of the final product that may
puncture wounds on fruit usually har- Technologies in turn contaminate the kitchen of the
bor greater numbers of pathogens to unaware consumer. A new method of
greater depths than seen at other loca- Preservation techniques currently heating food (e.g., microwave) may speed
tions of the intact fruit (Burnett et al., act in one of three ways: (1) preventing up the heating and change the types of
2000). More significant, Burnett et al. pathogen access to foods, (2) inactivat- microorganisms that survive the heating
(2000) found that a negative temperature ing them should they gain access, or (3) process, whether the heating takes place
differential (application of cold rinse wa- preventing or slowing their growth in a food processing plant or the con-
ter to warm fruit) may increase the rela- should the previous two methods fail sumer’s kitchen.
tive attachment and infiltration of bacte- (Gould, 2000a). Traditional food pro-
rial pathogens in intact fruit. This obser- cessing has relied on thermal treatments Overview
vation has significance for the use of hy- to kill/inactivate microbiological con-
drocooling technology, which has been taminants. Unfortunately, thermal pro- A recent report generated by IFT for
applied to produce items such as straw- cessing induces physical and chemical FDA (IFT, 2000b) defined alternative
berries, cherries, and field crops. Al- changes in the food. Canned green technologies, identified the pathogens of
though hydrocooling water is frequently beans do not have the same taste and public health concern that are the most
decontaminated by chlorination, inade- texture as fresh, despite having similar resistant to various technologies, de-
quate control of pathogens in water re- nutritional profiles. Chemical preserva- scribed the mechanisms of pathogen in-
circulated through hydrocoolers could tives and naturally occurring antimi- activation including the inactivation ki-
provide a source of pathogens that then crobial compounds also have been used netics, identified ways to validate the ef-
infiltrate produce items because of the extensively for food preservation fectiveness of microbial inactivation,
temperature differentials. (Davidson, 1997). Again, a “pickled” or identified critical process factors, and
Historically, water for food process- acidified food such as cauliflower does described process deviations and ways
ing in the United States has originated not have the same role on the menu as a to handle them. The report also de-
from municipal systems. However, with fresh stalk of cauliflower, despite their scribed synergistic effects among tech-
increased volume, as well as stricter reg- identical origin. Beyond the use of sin- nologies, when data were available, and
ulations, water usage in the processing gular food preservation techniques, articulated future research needs for
environment has increased dramatically many strategies employ a combination each technology.
over the last decade. Water reclamation of preservation techniques, e.g., refriger- Kinetic parameters and models are
and reuse has received considerable at- ated storage under modified atmo- frequently used to develop food preser-
tention, with guidelines provided by the sphere, reduced heat treatment with vation processes that ensure safety. They
Environmental Protection Agency (EPA) some acidification, and mild heat with also allow scientists to compare the abili-
(EPA/AID, 1992), although actual stan- reduced water activity (Gould, 2000b). ty of different process technologies to re-
dards remain the responsibility of state Leistner (2000) states that the impor- duce microbial populations. Kinetic pa-
agencies. These EPA guidelines address tant preservation approaches often use rameters, with their recognized limita-
water reclamation for nonpotable urban, combinations of several factors to as- tions, use empirical coefficients experi-
industrial and agricultural reuse; direct sure microbiological safety. These fac- mentally determined from microbial re-
potable reuse is not practiced in the tors, often called “hurdles,” include heat, duction measurements to document the
United States. Food processors have ex- acidity, water activity, redox potential, relationship between microbial popula-
pressed some interest in water reuse as preservatives, competitive flora, low tion decreases and different process con-
well, particularly in animal slaughter fa- temperatures, and more than 40 other ditions. Kinetic parameters for microbial
cilities and the USDA/FSIS has issued possible factors. Increasingly, the Amer- populations exposed to thermal treat-
guidance for this application. In general, ican public has sought “fresh” products, ments have been assembled over a signif-
the reuse of water from any one location fueling efforts to develop many alterna- icant period of time. Published literature
in the slaughter process is restricted to tive processing technologies that result has included kinetic parameters needed
certain other point locations in the in products that have minimal process- to control most process, product and mi-
slaughter process, as provided by specific induced changes in sensory and nutri- crobial situations (Pflug and Gould,
recommendations of the agency. In al- tional characteristics. It is expected that 2000).
most every instance, decontamination these technologies will play an increas- IFT (2000b) used the models and ki-
steps such as addition of chlorine, as well ing role in food processing in the future. netic parameters to present and compare
as microbiological monitoring, must be Any discussion of emerging food microbial inactivation data from ther-
done on the reconditioned water, with safety issues must consider the impact of mal, pressure and electromagnetic pro-
very specific standards recommended. these alternative food processing tech- cesses. Thermal parameters apply to mi-
Reuse water from advanced wastewater nologies. This analysis must consider crowave energy, electrical resistance

(ohmic), and other temperature-based wave energy and ohmic technologies. estimated, highlighting the urgent need
processes. Researchers have spent sub- The parameters currently used for pres- for additional research. For several other
stantial time studying how various mi- sure or pulsed electric field (PEF) treat- technologies, the quantity of data de-
crobial populations respond to thermal ments should be applicable to other pro- scribing the treatment’s reduction of mi-
treatments. The scientific literature con- cesses where pressure or electricity is the crobial populations is insufficient for a
tains kinetic parameters for most pro- primary critical factor in reducing mi- comparison.
cess, product and microbial situations. crobial populations. Given the scarcity Scientists face limitations in inter-
These thermal parameters provide a of data, parameters for pressure or preting these parameters. When the pa-
sound basis for development of micro- pulsed electric field treatments must be rameters are used to develop a process,

Table 10. Limitations to Alternative Processing Technologies Currently Under Development (IFT, 2000b)

Limitations applicable to all or most of the technologies:

Linear first-order survivor curve model Different inactivation action/mechanism(s) No reliable methods for measuring and
may be inadequate. Appropriate model(s) among alternative technologies unidentified monitoring temperatures or other treatment
would be beneficial to all preservation and undefined to date. actions within individual, large, solid
technologies. particulates.
Synergism or antagonism of one alternative
Standardized experimental protocol(s) for process used with another and their combined Possible new or changing critical process
obtaining statistically reliable kinetic effect on microbial inactivation efficiency factors and their effect on microbial
parameters to describe survivor curves for undetermined to date. inactivation.
microbial populations exposed to various
Potential formation of unpalatable and toxic
alternative technologies.
by-products due to processing.

Pulsed Electric Field: Electrothermal: among pressure, temperature and other

variables unknown.
Few published reports Difficult to monitor temperature distributions and
heating patterns in solids and particles High capital costs of equipment
Kinetics based on 2-point survivor curves
No well-developed models for process deviations Questionable reliability of equipment
Few reports state threshold field strength and use of alternative or variable frequencies of
for inactivation Solid food must be batch processed and
processing energy
pumpable foods only semi-continuous
Treatment vessel design is major variable Some food factors influence process effectiveness
among studies Minimal inactivation of bacterial spores in low-
Most resistant pathogens and appropriate acid foods unless mild heat is applied
Mechanisms of action need confirmation surrogates need to be identified
Survival curves often nonlinear complicating
Most resistant pathogens and appropriate Development of resistance after sublethal kinetics and calculation of process parameters
surrogates need to be identified treatment needs to be tested
Food enzymes respond differently from each
Development of resistance after sublethal Kinetic models and critical process factors other
treatment needs to be tested affecting kinetics are needed
Excessive pressure denatures proteins and
Kinetic models and critical process factors High Pressure Processing: changes food
affecting kinetics are needed
Influence of pressure on reduction of microbial Most resistant pathogens and appropriate
Effective monitoring systems, uniform populations using the proper experimental surrogates need to be identified
treatment chamber design, electrode design (statistically valid, collection of data at
Development of resistance after sublethal
construction, and other hardware different pressures and control of temperature
treatment needs to be tested
components are needed to assure and product), so that z(P) (increase in MPa to
consistent delivery of specified reduce D value by factor of 10) and/or activation Kinetic models and critical process factors
treatment volumes (V) are quantified. Synergistic effects affecting kinetics are needed

Some of the technologies present greater need to be developed before consideration for especially in treating water and fruit juices. A
limitations than others or are at a use in food preservation. Likewise, oscillating 4-log bacterial reduction was obtained for a
development stage that requires extensive magnetic fields have been explored for their variety of microorganisms when 400 J/m2
further scientific research before they can potential to inactivate microorganisms. was applied. Apple cider inoculated with E.
be commercially used. For these However, the results are inconsistent; different coli O157:H7 treated in that manner achieved
technologies, data are insufficient to studies have shown the level of microorgan- a 5-log reduction. To achieve bacterial
calculate kinetic parameters. For isms may increase, decrease or not be affected. inactivation, the UV radiant exposure must be
example, high voltage arc discharge Data on inactivation of food microorganisms by at least 400 J/m2 in all parts of the product.
(application of discharge voltages through ultrasound (energy generated by sound waves Critical factors include the transmissivity, the
an electrode gap below an aqueous of 20,000 or more vibrations per second) are geometric configuration of the reactor, the
medium) causes electrolysis and highly scarce and limitations include the inclusion of power, wavelength and physical arrangement
reactive chemicals. Although microorgan- particulates and other interfering substances. of the UV source, the product flow profile, and
isms are inactivated, more recent designs Ultraviolet light (UV) is a promising technique radiation path length.


care should be taken to compare the re- extensive treatment than those that are that applying pressure in this manner in-
sistance of different microbial popula- pasteurized. This goal must be consid- activated microorganisms and could be
tions or to identify the appropriate target ered when evaluating alternative process- used to preserve foods (Hite, 1899).
microorganisms. When a new alternative ing technologies as well. Larsen and coworkers (1914) confirmed
processing technology is under review, it Development of a number of alterna- that high pressure processing (HPP) can
is essential to determine the pathogens of tive processing technologies is underway, kill microbial cells. Vegetative bacteria
greatest public health concern. although many of these technologies re- were inactivated after 14 hours at 607
When exploring the new preserva- quire additional research before they are MPa; bacterial spores were extremely re-
tion technologies, their preservation level ready for commercial application (see Ta- sistant to pressure but could be inacti-
should be compared to that of classical ble 10). Validation of effectiveness is an vated at 1,214 MPa. Today, HPP of foods
thermal pasteurization or commercial important step in the development of any uses pressures within the range of 300 to
sterilization technologies. Thermal pas- new technology (see sidebar below). 700 MPa.
teurization focuses on inactivating vege- Over the last fifteen years, use of
tative cells of pathogenic microorgan- High Pressure Processing HPP as a food preservation method has
isms, i.e., microbial cells that are not dor- been pursued in an effort to produce safe
mant, highly resistant spores. However, To preserve food using high hydro- foods with a reasonable shelf life with the
to have a commercially sterile product, static pressure, the food (normally pack- use of minimal heat. Reducing or elimi-
the process must control or inactivate aged) is submerged in a liquid (usually nating high temperatures in food pro-
any microbial life (usually targeting water) contained in a vessel that gener- cessing can deliver a food product with
spores of C. botulinum) capable of ger- ates pressure by pumping more liquid flavor, texture, appearance, and nutrient
minating and growing in the food under into the pressure vessel or reducing the content very similar or identical to fresh
normal storage conditions. Commercial- volume of the pressure chamber. or raw food. The first commercial prod-
ly sterile products generally require more In the 19th century, scientists realized ucts treated by HPP—fruit products

Validation of Treat-
well-defined characteristics and a long tual plant conditions, which includes
ment Effectiveness history of being nonpathogenic. It can be processing and control equipment,
especially difficult to identify surrogates product handling and packaging. Be-
Using Microbiological that are not pathogenic for highly suscep- cause pathogens should not be intro-
tible subpopulations and that are unlikely duced into the production area, surro-
Surrogates to undergo transformation into a patho- gate microorganisms should be used in
The function of surrogate organ- genic phenotype in the production envi- inoculated pack studies, and their sur-
isms is different from that of microbio- ronment. In selecting surrogates, the fol- vival or growth can be measured to
logical indicators. Surrogates are used lowing microbial characteristics are desir- validate the process. For instance, sur-
to evaluate the effects and microbial re- able: rogates have been used for many years
sponses to processing treatments. The • Nonpathogenic in the low-acid canning industry to es-
main difference between surrogates and • Inactivation characteristics and ki- tablish and validate the destruction of
indicators is that the latter is naturally netics that can be used to predict those of C. botulinum spores. The use of non-
occurring and the former is introduced the target organism pathogenic spores of the putrefactive
as an inoculum. In the case of fresh • Behavior similar to target microor- anaerobe Clostridium sporogenes, or
and fresh-cut produce where no tradi- ganisms when exposed to processing pa- spores of the flat-sour thermophilic or-
tional processing inactivation steps are rameters (for example, pH stability, tem- ganism Bacillus stearothermophilus as
used (e.g., heat pasteurization), surro- perature sensitivity, and oxygen toler- surrogates for C. botulinum, have
gates could be used to assess and vali- ance) helped the industry develop thermal
date decontamination procedures. In • Stable and consistent growth charac- processes that ensure products are safe
the case of alternative processing tech- teristics and commercially sterile. Listeria in-
nologies, surrogates could be used to • Easily prepared to yield high-density nocua M1 has thermal resistance pro-
validate specific processing efficacy and populations files similar to L. monocytogenes but is
treatment delivery. Surrogates may be • Once prepared, population is con- designed for easy detection as a surro-
selected cultures prepared in a labora- stant until utilized gate and is not a pathogen (Fairchild
tory and inoculated onto or into the • Easily enumerated using rapid, sen- and Foegeding, 1993). In addition,
product, or they may be an inoculum sitive, inexpensive detection systems nonpathogenic strains of E. coli have
of naturally occurring microorganisms • Easily differentiated from other mi- served as surrogates for E. coli
that conforms to the requirements of a croflora. O157:H7. In all cases, the surrogate
surrogate and has been confirmed to The validity of an established or new organism is added to the food product
exist at adequate concentrations in the preservation or decontamination process and used to obtain quantitative infor-
specific product. Generally, surrogates is frequently confirmed using an inocu- mation to determine and validate the
are selected from the population of lated test pack consisting of the food efficacy of food processing or decon-
well-known microorganisms that have product inoculated and tested under ac- tamination methods.

such as jams and jellies—reached the is one of the primary reasons for loss of cant reduction in microbial population.
marketplace in Japan in 1991. An acidic membrane integrity leading to injury Pressures greater than 500 MPa are
pH is an important element in the safety and death of the bacterial cell (Paul and usually required for greater microbial re-
of HPP preserved foods because the Morita, 1971). Pressure-induced mal- duction or consistent product steriliza-
pressures used in commercial applica- functions of the membrane inhibit ami- tion, but use of low pH and mild heat
tion of the technology have limited effec- no acid uptake that is probably due to treatment (45 – 70 C) is often necessary
tiveness against bacterial spores. membrane protein denaturation, but it to attain commercial sterility. For exam-
Certain principles apply to HPP in- has been shown that bacteria with a rela- ple, in the case of green infusion tea,
activation of pathogenic bacteria: (1) in- tively high content of diphosphatidyl- Kinugasa et al. (1992) produced a com-
creasing the pressure magnitude or time glycerol (shown to cause rigidity in mercially sterile product using 700 MPa
of pressurization will usually increase membranes in the presence of calcium) at 70 C for 10 minutes. These treatment
the number of bacteria destroyed (with are more susceptible to inactivation by parameters were successful even when
the exception of bacterial spores); (2) an HPP (Smelt et al., 1994), and those com- the tea was inoculated with 106 spores of
acidic pH or temperatures above ambi- pounds that enhance membrane fluidity B. cereus, Bacillus coagulans and Bacillus
ent enhance pressure inactivation rates; usually impart pressure resistance to an licheniformis. The tea’s flavor was un-
(3) gram-positive bacteria tend to be organism (Russell et al., 1995). It is well changed as were the catechins, vitamin C
more resistant to HPP than gram-nega- established that a loss of intracellular and amino acids in the tea. In another
tive bacteria; (4) cells in exponential components occurs when microorgan- example of using HPP in a combined
phase are generally more pressure-sensi- isms are exposed to high levels of hydro- preservative approach, Shearer et al.
tive than in stationary phase; and, (5) in- static pressure. (2000) measured the reduction of spores
complete inactivation of bacteria using Some foodborne pathogens are more of Bacillus, Clostridium and Alicycloba-
HPP can result in injured cells that are resistant to inactivation by HPP than cillus in test foods using HPP and 45 C
capable of recovery under optimal others. In work by Patterson et al. (1995), in combination with such preservatives
growth conditions, a common phenome- Yersinia enterocolitica was reduced 5 log10 as sucrose laurates, sucrose palmitate,
non known as sublethal injury. cycles when exposed to 275 MPa for 15 sucrose stearates, and monolaurin. Oth-
Although increasing the pressure minutes in a phosphate-buffered saline er preservative combinations that in-
kills more bacteria in less time, higher solution. For comparable 5-log10 reduc- clude HPP also used carbon dioxide
pressures can cause far greater levels of tions using 15-minute treatments, S. Ty- (Haas et al., 1989) and acidification plus
protein denaturation and other detri- phimurium required 350 MPa, L. mono- addition of nisin (Roberts and Hoover,
mental changes in sensory quality that cytogenes required 375 MPa, S. Enteriti- 1996).
affect the food’s appearance and texture dis required 450 MPa, and E. coli HPP continues to be developed as a
as compared to the unprocessed product. O157:H7 and S. aureus required 700 nonthermal food processing method;
The major factors affecting the effec- MPa. The bacteria showed more pres- however, scientists still need to develop a
tiveness of HPP are: the type of bacteria sure resistance in ultra high temperature reliable method to predict the HPP pro-
present in the food; its growth condi- processed milk than meat or buffer. cess endpoint, the point at which all
tions; the composition, pH and water ac- Thus, the variability of pressure response pathogenic bacteria are inactivated. The
tivity of the food; and the temperature, is related to bacterial differences and dif- heat resistance of a pathogen does not
magnitude, and time of pressurization ferent food substrates. By using treat- directly correlate to its pressure resis-
(Hoover, 1993). ment temperatures of 50 C instead of tance, and the potential emergence of
As described by LeChatelier’s Princi- ambient, similar reductions could be ac- pathogens with unusual pressure resis-
ple, pressure enhances reactions that re- complished for E. coli and S. aureus at tance is an issue to address. As a relative-
sult in a volume decrease and inhibits 500 MPa instead of 700 MPa (Patterson ly new commercial food process, concern
those reactions leading to an increase in and Kilpatrick, 1998). still exists for the safety of some foods
volume (Johnson and Campbell, 1945). For most foods, 10-minute expo- processed using HPP, especially given the
For this reason, pressure alters the equi- sures to pressures in the range of 250- ever-evolving nature of microorganisms.
librium of the interactions that stabilize 300 MPa (37,500-45,000 psi) result in
the folded three-dimensional shape of what can be called “cold pasteurization.” Irradiation
proteins (Masson, 1992). The extent of Here, levels of inactivation represent a
denaturation by pressure depends upon reduction of microorganisms (primarily Food irradiation, first commercially
the structure of the protein, the pressure vegetative bacteria) of approximately 4 to introduced in the early 1960s, uses ioniz-
range, and other external parameters 6 log10 CFU/mL or g. Cold pasteuriza- ing radiation to decontaminate and dis-
such as temperature, pH and solvent tion is a currently popular term used infect food and inhibit sprouting and
composition. Pressure will primarily af- widely for any “nonthermal” food pro- ripening. The ionizing radiation is usual-
fect the hydrophobic interactions of pro- cess or processes (such as HPP or irradi- ly in the form of gamma rays produced
teins; covalent bonds are not affected. ation) that do not depend on extensive by radionuclides such as 60Co (cobalt) or
Consequently, the extent of hydropho- heat as the major mechanism of microbi- 137
Cs (cesium). Newer irradiation tech-
bicity of a protein can significantly deter- al inactivation. Foods that are cold-pas- nologies include e-beam, where ordinary
mine the degree of protein denaturation teurized are not cooked or heated in the electricity is used to produce a stream of
at any given pressure (Jaenicke, 1981). conventional sense and thus do not sig- electrons, or x-ray irradiation, where the
Pressurized membranes normally show nificantly lose sensory quality (e.g., ap- electron beam is bounced off metal to
altered permeabilities and it is believed pearance, texture, and flavor) and nutri- create x-rays (Farkas, 1998). To get away
that denaturation of membrane proteins ent content; however, there is a signifi- from using the term “irradiation,” food


irradiation is more frequently referred to accepted by FDA for food safety purpos- food irradiation. However, as irradiation
as cold pasteurization, because the much es include the more recent addition of becomes more widely used, the potential
shorter wavelengths of gamma and x- microbial control in fresh and frozen for the production of resistant pathogen-
rays and e-beams penetrate the food very meat and poultry. ic mutants could be magnified, so con-
rapidly and little or no heat is produced. To establish the safety of a proposed tinued surveillance is warranted.
The purpose of food irradiation depends food irradiation application, FDA re- Treatment with low to medium doses
on specific applications; in general, food quires data on the radiological, toxico- (i.e., non-sterilizing doses) of ionizing
irradiation is used to reduce the levels of logical, and microbiological safety, as radiation greatly reduces, but does not
foodborne pathogens on the food, inacti- well as the nutritional wholesomeness of necessarily eliminate, bacteria and other
vate the food spoilage microorganisms, the irradiated product (Pauli and Taran- organisms that may be present in the
and prolong the shelf life of fresh foods tino, 1995). From the perspective of ra- food (Monk et al., 1995). Complete ster-
by decreasing the normal biological diological safety, the energy produced by ilization of foods is not the purpose nor,
changes associated with growth and mat- approved radiation sources is too low to in most cases, even desirable for irradia-
uration processes, such as ripening or induce radioactivity in foods. The issue tion. Because non-sterilizing doses of ra-
sprouting. Both gamma irradiation and of toxicological safety is more complex diation do not kill all bacteria, certain
x-rays can be used for thick foods as they and has been thoroughly studied in the pathogenic bacteria (e.g., C. botulinum,
penetrate several feet, whereas e-beam ir- past. Recent petitions in the meat and Salmonella) may survive and, in the ab-
radiation can only penetrate several poultry area have indicated that FDA’s sence of competition from harmless bac-
inches. As well, both e-beam and x-ray principal current interest lies in specifi- teria, may multiply to potentially hazard-
irradiation are considered environmen- cation of the conditions for food irradia- ous levels. Before using irradiation as a
tally friendly, due to the absence of a ra- tion (such as temperature and packaging food safety measure, experimental evi-
dioactive power source and the ability to atmosphere) and their impact on micro- dence is required to demonstrate that the
switch the system off and on at will. biological safety and nutritional adequa- proposed treatment achieves the intend-
FDA has expanded the use of x-ray cy (Olson, 1998). The two most impor- ed microbiological control without al-
and e-beam irradiation for the treatment tant concerns related to the microbiolog- lowing C. botulinum growth and toxin
of prepackaged foods, and companies in ical safety of irradiated foods are (1) the production.
the United States have recently begun us- potential to create highly virulent mutant Most of the recent interest in food ir-
ing e-beam technology to pasteurize pathogens, and (2) the potential that re- radiation has focused on its efficacy in
ground beef. In addition, companies in ducing the harmless background microf- controlling bacterial pathogens such as
the United States will soon begin using lora could eliminate competitive micro- Salmonella, E. coli O157:H7 and L.
x-ray systems for irradiation of packaged bial forces and allow uncontrolled monocytogenes in muscle foods. As with
foods. For example, a new x-ray test cen- pathogen growth. heat, higher irradiation doses kill greater
ter has opened, allowing food producers The relative radiation resistance of numbers of bacteria (Olson, 1998).
to fine-tune x-ray irradiation protocols microorganisms can be summarized as While different bacterial species and
for a variety of foods. follows (in order of most resistant to strains demonstrate differences in rela-
Like other physical processes such as least resistant): viruses>spores>gram- tive radiation resistance, recommended
cooking and freezing, irradiation can positive bacteria>gram-negative irradiation doses for fresh meat and
cause some alteration of the chemical bacteria>yeasts and molds>parasites poultry result in destruction of greater
and sensory profiles of a food. Treatment (Monk et al., 1995). However, there are than 99.9% of Salmonella and L. mono-
with ionizing radiation results in chemi- some nonsporeforming bacteria, such as cytogenes, and more than adequate con-
cal modification of extremely small Deinococcus radiodurans and Acineto- trol of E. coli O157:H7 (Farkas, 1998; Ol-
amounts of the major constituents of bacter radioresistens, that are extremely son, 1998). The marine Vibrio patho-
food (carbohydrates, proteins and lip- radiation resistant by virtue of their ge- gens, of concern in bivalve molluscan
ids), and can also affect minor compo- netic make-up. Although the exact cel- shellfish, are also extremely radiation-
nents of food, specifically vitamins and lular mechanism(s) responsible for such sensitive (Rashid et al., 1992). The para-
DNA. However, these changes are con- resistance is unknown, scientists believe site T. gondii is readily inactivated by
sidered insignificant with respect to nu- that these radiation-resistant bacteria gamma irradiation at doses of 0.25 kGy
tritional adequacy. In general, most food possess particularly effective nucleic acid (Dubey et al., 1986), whereas T. spiralis is
nutrients are unaffected by irradiation, repair mechanisms. Although these or- more resistant to gamma irradiation and
with the exception of some vitamins for ganisms are not known to be pathogens, requires doses of 7-9.3 kGy to kill the
which minor decreases may occur. It is they may provide a genetic pool from parasite in situ and 0.18 kGy to stop de-
unlikely, however, that any vitamin defi- which pathogens could theoretically pick velopment of larvae to the adult stage
ciency would result from the consump- up resistance genes through mechanisms (Monk et al., 1995). Unfortunately,
tion of irradiated foods (Diehl, 1995; Jo- of genetic exchange. Furthermore, some foodborne viruses such as hepatitis A vi-
sephson et al., 1978; Kilcast, 1994). researchers have proposed concerns that rus and the Norwalk-like viruses are re-
U.S. commercial production of irra- irradiation may produce mutant strains sistant to radiation inactivation, and this
diated foods for food safety purposes is and/or radiation-resistant pathogens by is not a promising control technology for
relatively recent, although the technology means of natural selection. To date, vari- these foodborne pathogens (Bidawid et
has a longer history as a treatment for ous studies and independent reviews by al., 2000; Mallett et al., 1991).
medical devices and for control of insect researchers and international organiza- Besides having an effect on pathogen
infestation and sprouting in fresh pro- tions have found no indication of specif- load, an added benefit of irradiation is a
duce. Applications of ionizing radiation ic bacteriological hazards associated with reduction in the numbers of spoilage mi-

croorganisms. For instance, the gram- be addressed as food irradiation facilities optimal gas composition and humidity
negative psychrotrophs, which are the are established. For example, the occupa- level. The challenge for food manufac-
predominant spoilage organisms for tional health and safety of workers in ir- turers is to maintain product safety while
fresh meat and poultry, are very suscep- radiation facilities and the transport of providing these storage and preservation
tible to irradiation. In general, irradia- radioactive materials for gamma irradia- conditions.
tion of raw meats results in a significant tion facilities merit consideration. If Ideally, active packaging would sense
extension of shelf life, as much as twice gamma irradiation of food becomes a the microenvironment within the pack-
that of non-irradiated, refrigerated significant industry in the future, it will age and modify conditions accordingly
products (Olson, 1998). However, re- likely entail the construction of more fa- to extend shelf life, improve safety or en-
gardless of the impact of food irradia- cilities and the increased transport of ra- hance sensory properties. This active ap-
tion on reducing spoilage and bacterial dioactive materials. These concerns may proach is different but complementary to
pathogens, proper storage and handling, increase advancement of the more envi- intelligent packaging, which provides in-
including temperature control, after ronmentally friendly irradiation technol- formation about critical parameters such
processing is necessary to ensure that ogies, namely x-ray and e-beam irradia- as temperature, time, gas content, or mi-
the food will be safe. It also should be tion. crobial contamination. New packaging
noted that the effect of irradiation treat- There is also a need to do more work advances are starting to combine these
ments on the sensory qualities of foods on indicators that one can use to deter- two concepts in the next generation of
depends largely on the type of food mine if foods have been irradiated and if food packaging.
product undergoing treatment, as well so, the level of irradiation given. At the Active packaging is not one technolo-
as the dose of radiation used. In some recommended doses for specific applica- gy, but a collection suited to specific
instances, the dose of radiation neces- tions, there are no major chemical, physi- problems. Active packaging concepts can
sary to destroy pathogens produces un- cal, or sensory changes in irradiated be divided into three major categories:
desirable organoleptic changes in the foods. Therefore, detection methods modified atmosphere packaging, active
food product. For example, oxidation of must focus on minute changes such as scavenging (oxygen, ethylene, carbon di-
lipids in the food can cause discolora- minor chemical, physical, histological, oxide) and releasing concepts [emitters
tion and rancidity. In short, irradiation morphological, and biological changes in (carbon dioxide, ethanol, flavors, fra-
is not an effective treatment for patho- the food. Some promising methods for grances), and microbial control systems
gen control in all food products. measuring these changes in food include (chlorine dioxide, sulphur dioxide)].
Irradiation represents one tool hydrocarbon and cyclobutone for lipid-
among several (e.g., fumigants, carcass containing foods, electron spin reso- Modified Atmosphere Packaging
rinses, steam pasteurization, chemical nance for bone-containing food, ther-
sprout inhibitors, food preservatives) for moluminescence for foods containing Modified atmosphere packaging
enhancing food safety. It is likely that in silicate minerals (Olson, 1998) and the (MAP) involves the creation of a modi-
the future, food irradiation would be DNA comet assay for analysis of foods fied atmosphere by altering the normal
used to complement rather than replace with low fatty acid content (Cerda et al., composition of air (78% nitrogen, 21%
many of the other techniques already in 1997). oxygen, 0.03% carbon dioxide and traces
use. Alternatively, combination treat- of noble gases) to provide an optimum
ments in line with the hurdle concept Active and Intelligent Packaging atmosphere for increasing the storage
(e.g., irradiation plus MAP) may be- length and quality of food (Moleyar and
come more commonplace and offer an The primary purpose of food pack- Narasimham, 1994; Phillips, 1996). The
additional level of control. In some cas- aging is to protect the food from physical, atmospheric modification can be
es, irradiation may be a safer alternative. microbial and chemical contamination. achieved by using controlled atmosphere
For example, when used to reduce the Therefore, the type of packaging used storage (CAS) and/or active or passive
microbial load on spices, irradiation can plays an important role in determining MAP. Active modification creates a slight
serve as an alternative to fumigants such the shelf life of a food. Today’s consum- vacuum inside the package that is then
as ethylene oxide or methyl bromide, ers increasingly demand mildly pre- replaced by a desired mixture of gases.
which are particularly toxic to occupa- served convenience foods with fresh-like Passive modification occurs when the
tionally exposed individuals. qualities. In addition, advances in retail product is packaged using a selected film
A key advantage of food irradiation and distribution practices (e.g., central- type, and a desired atmosphere develops
for controlling pathogens is that it re- ization of activities, Internet shopping, naturally as a consequence of the prod-
duces the microbial load at the point at global procurement) lead to greater dis- uct’s respiration and the diffusion of gas-
which the product has been packaged, tribution distances and longer storage es through the film (Lee et al., 1996; Mo-
which increases the likelihood that the times for a variety of products with dif- leyar and Narasimham, 1994; Zagory,
product the consumer receives will be ferent temperature requirements, thereby 1995). The choice of the film is an inte-
safe. However, like other processes, irra- creating immense demands for innova- gral part of this system, because gas dif-
diation only protects against pathogens tion from the food packaging industry. fusion rates vary greatly among films,
that contaminate the product at the time Active and intelligent packaging technol- and therefore films differ in their ability
of processing; it does not protect against ogies are used to extend shelf life, im- to maintain the desired modified atmo-
future contamination that may occur prove safety and improve the sensory sphere. Also taken into consideration is
during handling, storage and prepara- properties of packaged foods. This is the storage temperature, which will also
tion of the food. achieved by providing the best microen- affect gas diffusion rates.
A number of additional issues must vironment within the package through The increased product shelf life re-


sults from the effect of the modified en- may pose a food safety concern. A low scavengers is that they can reduce oxygen
vironment on microbial growth and, for partial pressure of carbon dioxide, com- levels to less than 0.01%, which is much
respiring food products such as fruits bined with refrigerated storage, can also lower than the typical 0.3-3.0% residual
and vegetables, on the product (Molin, favor the growth of Aeromonas and the levels achievable with modified atmo-
2000). Low oxygen levels negatively af- Enterobacteriaceae. MAP containing el- sphere packaging. As well, oxygen scav-
fect aerobic microorganisms. Carbon di- evated levels of CO2 (70-100%) inhibits engers are sometimes used in combina-
oxide inhibits the growth of some micro- the growth of L. monocytogenes in a va- tion with carbon dioxide scavenger sys-
organisms, however, it is not inhibitory riety of products (meat products, cot- tems.
for all microorganisms, and it is impor- tage cheese, turkey roll slices), whereas In terms of public health, the main
tant to understand that under modified 100% N2 allows multiplication of the issue surrounding the use of oxygen
atmospheres, the growth rates of some pathogen (Phillips, 1996). Fresh-cut scavengers is their potential to create an
microorganisms will be reduced, while and whole fruits and vegetables, in par- environment that may promote the
others may increase or stay the same. ticular, do not usually tolerate CO 2 con- growth of potentially harmful anaerobic
MAP is not without safety concerns. centrations above 15%, well below the bacteria. Similar concerns have been dis-
Beneficial microorganisms may be in- inhibitory level for L. monocytogenes. cussed with respect to MAP conditions
hibited, potentially allowing certain The CO2 rich atmosphere, however, can that result in a low oxygen atmosphere
pathogens to proliferate and cause select for lactic acid bacteria, which have within the package. The main organisms
foodborne illness. C. botulinum, L. been shown to be inhibitory towards L. of concern in this situation are Clostridi-
monocytogenes and potentially patho- monocytogenes (Francis and O’Beirne, um species, mainly C. botulinum, but also
genic psychrotrophs are of primary 1998). C. perfringens, due to their growth and
concern. Psychrotrophs grow well at or toxin production in anaerobic environ-
below 7 C and have their optimum Active Scavenging Concepts ments.
growth temperature between 20 and 30
C, meaning they can multiply under re- Active scavenging concepts include Active Releasing Concepts
frigeration conditions. If the oxygen lev- oxygen, ethylene and taint scavengers as
el of the modified atmosphere is too well as moisture absorbers or humidity Considerable research has focused
low, the anaerobic environment could controllers. on the release of antimicrobials from
facilitate C. botulinum growth. Al- The presence of oxygen in food pack- packaging materials to limit microbial
though studies indicate that many foods ages accelerates the spoilage of many spoilage, however the choice of antimi-
become inedible before any toxin is pro- foods. Although vacuum packaging and crobial compound is often limited by its
duced (Molin, 2000), foods that remain MAP have been somewhat successful in compatibility with the packaging materi-
organoleptically acceptable after toxin extending the shelf life and quality of al and by the ability to withstand the heat
production are a significant public food, aerobic spoilage can still occur be- during extrusion (film formation). Ex-
health concern. For example, recent cause of residual oxygen in the head- amples of such compounds are chlorine
studies have shown that C. botulinum space. Oxygen residual remains due to dioxide, sulphur dioxide, ethanol, carbon
can grow and produce toxin in products oxygen permeability of the packaging dioxide emitters, antimicrobials (zeolite,
such as MAP pizza and English-style material, small leaks due to improper triclosan and bacteriocins) and antioxi-
crumpets, while the products remain sealing, air enclosed in the food or inade- dants (BHT/BHA or vitamin E).
organoleptically acceptable (Daifas et quate evacuation and/or gas flushing.
al., 1999a,b). With respect to meat and Oxygen can cause off-flavors, color Intelligent Packaging Systems
fish products, Molin (2000) concluded change, nutrient loss, and growth of mi-
that most products are judged inedible croorganisms. Oxygen scavengers are Intelligent packaging can sense the
well before any toxin is produced. How- useful for removing residual oxygen and environment and/or convey information
ever, there have been studies where toxin can be applied in different ways: sachets to the user about its contents. Although
production in MAP meats preceded or and labels containing oxygen-scavenging research in this area has been extensive,
coincided with the development of un- components, closures (mainly used for only a few technologies have made it past
acceptable sensory characteristics plastic beer bottles), and oxygen-scav- the research and development phase. Two
(Lawlor et al., 2000), as well as reports enging flexibles. One of the largest appli- main strategies are employed in the de-
of botulism due to consumption of vac- cations of oxygen-scavenging systems is velopment of a new intelligent packaging
uum-packaged smoked fish products mold control in packaged baked goods system: the use of novel materials and
(Korkeala et al., 1998). L. monocytoge- and cheese food packages. processes, and the application of elec-
nes is a problem with products, such as The majority of current commercial- tronics and MEMS (microelectro-me-
ready-to-eat products, fruits and vege- ly available oxygen scavengers are based chanical systems). The first strategy is
tables, that are not heated adequately on the principle of iron oxidation. In- usually the least costly, but the develop-
before consumption. Low concentra- serting a sachet into the food package is ment and specification process can be
tions of CO2 (less than 10%) used in effective, but can meet with resistance time-consuming. Electronic or MEMS
MAP of some products may inhibit the among food manufacturers, because of technology is costly, but far more versa-
natural microflora and increase the fear of ingestion of the sachet, notwith- tile and flexible. The technology can be
growth rate of L. monocytogenes. Com- standing the labelling, and the potential used to micro-fabricate sensors that will
bined with storage at refrigeration tem- for the sachet to leak the contents into detect pressure, acceleration, humidity,
peratures, which can select for L. mono- food, resulting in an adulterated product. temperature, physical damage and expo-
cytogenes, a low-CO2 MAP environment The main advantage of using oxygen sure to radiation.

Key applications for intelligent tech- effects that new technologies have on the normally transported to holding, ship-
nology are in the areas of tamper evi- interrelationship among food, microor- ping, or processing facilities. Even pro-
dence, quality monitoring (i.e., tempera- ganisms and package is required. Ques- cessed foods that have received microbi-
ture abuse), counterfeiting (i.e., holo- tions remain about the by-products of cidal treatment are frequently transport-
grams), theft protection and supply oxygen-scavenging systems, the effective- ed to other locations for bottling, pack-
chain management and traceability (i.e., ness of antimicrobial films on products aging, and/or shipping. Transport con-
automatic data capture coupled to the with irregular surfaces, and the spectrum veyances are thus a part of the food
Internet). Traceability in the food chain of activity of the antimicrobial additives, chain where contamination can occur.
is a high profile issue, because of its im- to name a few examples. In addition to In 1994, an estimated 224,000 per-
portance in determining which foods are improving packaging technology, atten- sons developed salmonellosis from a na-
part of a potentially contaminated lot. tion must be given to fully understand- tionally distributed brand of ice cream
Tracing technology is already being used ing the effects on food quality and safety. (Hennessy et al., 1996). S. Enteritidis was
in many parts of the food chain, however, Active and intelligent packaging of- the cause, and the most likely scenario
a number of gaps exist. fer great benefits to both consumers was that pasteurized ice cream premix
An example of quality management and manufacturers and are undoubt- was transported by a tanker trailer that
packaging is a newly developed method edly one of the areas of future innova- had carried non-pasteurized eggs just
of preparing packaging material for food tion in the food industry. However, before being loaded with the premix.
and other products that contain diagnos- there are still concerns regarding the Eggs are a known source of S. Enteritidis.
tic properties. The technology involves regulatory approval of these technolo- The authors concluded that to prevent
immobilizing and protecting antibodies gies. Some of the packaging concepts, more such occurrences, food products
(or other ligands) on the polymer film such as the active release of antioxi- not destined to be re-pasteurized before
surface. These substances react with tar- dants or antimicrobials, have the po- use should be transported in dedicated
gets—such as food pathogens and tox- tential for these additives to migrate containers.
ins, pesticide residues or proteins in the into the food product. Food-contact As more and more food commodities
food—and create a visual sign on the approval must be established before are grown and harvested in the United
film surface, alerting the consumer or re- any form of active packaging is used, States and abroad, transportation will
tailer that the food may be contaminated. and labeling may be needed in cases continue to be a factor in foodborne ill-
However, this technology would likely where active packaging gives rise to ness and, in fact, may grow in impor-
only be applicable for surface contami- consumer confusion. As well, it is im- tance. This is not an easy issue to deal
nation. Other examples of quality man- portant to consider environmental reg- with, as the types of conveyances are as
agement technologies are temperature ulations covering disposal of active varied as the types of commodities they
indicators, time indicators (aging strip), packaging materials. Public perception transport.
time/temperature indicators, and micro- of antimicrobial or antioxidant use in The storage of foodstuffs also can be
wave cook indicators. food packaging must also be consid- an entry point for pathogenic microor-
ered. Consumers are seeking more ganisms or permit the growth of patho-
Future Directions and Concerns natural foods that are free of contami- gens if present. It is generally accepted
nants and additives, and their accep- that most foods need to be maintained at
From a human health and safety tance of packaging that incorporates cold temperatures from harvest to con-
standpoint, one must consider the effects these substances may be questionable. sumption. This “cold chain” is subject to
of active packaging on the microbial The use of natural antimicrobials, such abuse at several steps, and temperature
ecology and safety of foods. As previous- as those from plants, and natural anti- abuse can contribute to the growth of
ly discussed, removing oxygen from oxidants, such as vitamin E, in food pathogens that can increase the likeli-
within packs of high water activity, coatings or packaging may be more ac- hood of foodborne illness.
chilled, perishable food products may cepted by consumers. Storage of foodstuffs is carried out in
stimulate the growth of anaerobic patho- In the future, we will most likely see warehouses and specialized storage facil-
genic bacteria. In addition, the modified different combinations of active and in- ities, as well as in virtually all institutions
atmospheres created with MAP and scav- telligent packaging, e.g., combining an- that serve food, including hospitals,
enging technologies may sufficiently timicrobial films with MAP. Research is nursing homes, schools, restaurants, re-
change the competitive microbial envi- needed to see how these new packaging tail stores and the home. FDA has deter-
ronment, allowing for pathogen growth. technologies will impact on the spoilage mined that improper cold holding of
To control undesirable microorganisms microflora and survival/growth of food is the most frequent temperature
on food, antimicrobial substances can be foodborne pathogens. violation for nearly all facility types. For
incorporated into the surface of food With additional research, the combi- example, in a survey of fast food restau-
packaging materials. The major potential nation of active and intelligent packag- rants, 31% were out of compliance in
food applications for antimicrobial films ing technology may emerge as perhaps that potentially hazardous foods were
include meat, fish, poultry, bread, cheese, the most important preservation tech- being stored at temperatures above 41 F
fruits and vegetables. However, antimi- nology of the 21st century. (FDA, 2000).
crobial films that only inhibit spoilage The situation is no better, and is
microorganisms without affecting the Transportation and Storage probably worse, in the home setting. In a
growth of pathogenic bacteria, will raise recent survey of homes, 16% were hold-
food safety concerns that must be ad- Following the harvest of nearly all ing refrigerated ingredients at too high a
dressed. A better understanding of the commodity types, raw foodstuffs are temperature, and 55% of the participants


that were improperly holding cold ingre- food chain becomes even more com- in foodborne disease has been recog-
dients did not know at what temperature plex, perhaps their effect will become nized for years, recent food safety initia-
a refrigerator should hold product. The even greater. tives have increased our awareness of
remaining 45% of participants were un- particular risks. For instance, strong
aware that their refrigerators were not Retail and Food Service epidemiological evidence supports the
holding products at the proper tempera- transmission of Salmonella and Campy-
tures (Daniels et al., 2000). A previous The retail and food service environ- lobacter to ready-to-eat (RTE) food
survey showed that 23% of the 106 ments are part of the post-harvest envi- products via cross-contamination with
households had refrigerators that held ronment. As more meals are eaten away uncooked poultry (D’Aoust, 1989;
food at too high a temperature (Daniels, from home, this environment becomes Deming et al., 1987; Harris et al., 1986;
1998). increasingly significant. No matter how Hopkins et al., 1984). Equally strong
While improper transportation and well or how poorly food safety measures evidence exists for the transmission of
storage are hardly new or emerging are applied prior to consumption, avoid- viral foodborne disease by poor person-
food safety issues, they appear to be ing illness often depends on how well al hygiene of infected food handlers,
problems that do not go away. As such, food is handled immediately prior to with recent data suggesting that 50-95%
they will continue to contribute to the consumption. of confirmed viral foodborne disease
burden of foodborne illness. As the While the role of human handling outbreaks are attributable to human

Outbreaks of Shigella
but a high proportion of cases ate dishes outbreaks linked to this parsley source
sonnei Infection Associ- that were served with chopped parsley. suggested that the parsley was contam-
These results suggested that chopped inated in the field or during packing.
ated with Fresh Parsley parsley was the likely common source for However, results of these investiga-
In August 1998, the Minnesota De- the two restaurant outbreaks. tions also suggested that handling of
partment of Health (MDH) received In collaboration with CDC, other the parsley at the restaurants contrib-
multiple independent complaints of ill- public health agencies and public health uted to the occurrence of the out-
ness and reports of confirmed Shigella laboratories in the United States and breaks. Food handlers at six of the
infections among persons who had eat- Canada were notified of the outbreaks eight implicated restaurants reported
en at two restaurants (CDC, 1999c). in Minnesota. Six similar outbreaks washing the parsley before chopping it.
The restaurants were in different cities, that occurred during July-August were The parsley was usually chopped in
had separate water supplies, and had no identified, two in California, and one the morning and left at room tempera-
employees in common. Preliminary re- each in the states of Massachusetts and ture during the day before being
sults of interviews with patrons and Florida and the provinces of Alberta served to customers. Studies at the
food handlers at both restaurants sug- and Ontario. S. sonnei isolates were University of Georgia Center for Food
gested that ill food handlers likely available from five of these six out- Safety demonstrated that S. sonnei de-
played a role in contaminating ice and breaks. All had the same PFGE patterns creased by 1-log CFU/g per week on
fresh produce items. seen in the Minnesota outbreaks. In refrigerated parsley, but increased by
S. sonnei isolates from ill patrons each, chopped parsley was sprinkled on 3-log CFU/g in 24 hours on chopped
and food handlers at the two restau- foods that were either implicated by the parsley at room temperature. In addi-
rants were submitted to MDH for mo- results of a formal investigation, or eat- tion, in at least two of the restaurants,
lecular subtyping by pulsed-field gel en by a high proportion of cases. Thus, food handlers became infected with
electrophoresis (PFGE). Results of in simultaneous outbreaks linked by the outbreak strain of S. sonnei and
PFGE demonstrated that both restau- PFGE subtype, a common food item appeared to have contributed to ongo-
rant outbreaks were caused by the same was implicated. ing transmission in those outbreaks.
strain of S. sonnei and that it was a Tracebacks to determine the sources These outbreaks demonstrate the
strain that had not previously been iso- of parsley in the outbreaks linked by complexity of foodborne disease
lated in Minnesota. Strains with simi- PFGE were conducted by state and local transmission and outbreak investiga-
lar PFGE patterns had been isolated health officials, FDA, and the Canadian tions. A contaminated food ingredient
from travelers returning from Mexico. Food Inspection Agency. One farm, in was widely distributed, contamination
Because the outbreaks at the restau- Baja California, Mexico was identified as was amplified by handling practices in
rants appeared to have a common the likely source of parsley served in six some restaurants, and infected food
source, food histories of restaurant pa- of the seven outbreaks. Field investiga- handlers further amplified the out-
trons were re-evaluated by food ingre- tions at the farm found that municipal break by contaminating ice and other
dients rather than by menu item. In water used for chilling the freshly picked ready-to-eat foods. Only by linking
one restaurant, uncooked chopped parsley was unchlorinated and vulnera- this series of apparently unrelated out-
parsley was associated with illness ble to contamination. This water also breaks by PFGE subtyping of the
(odds ratio 4.3, 95% confidence inter- was used to make the ice with which the agent, were public health officials able
val 2.4, 8.0). In the other restaurant, parsley was packed for shipping. to identify the common source and the
parsley was not associated with illness, The widespread distribution of the other contributing factors.

handling (Bean et al., 1997). Another the propagation of a primary food- molds, and parasites—that may persist
particularly hazardous behavior is the borne viral disease outbreak. or grow in foods even if they do not ex-
consumption of high-risk foods (pre- perience sublethal injury. The activity of
dominantly raw or undercooked foods Microbial Stress Responses to the entire microbial ecosystem influences
of animal origin) (Beletshachew et al., Processing the survival and subsequent pathogenici-
2000; Klontz et al., 1995). ty of the target cells whether or not the
While all of these behaviors can oc- Human efforts to control microor- target microorganism has been suble-
cur at home, institutions and retail es- ganisms in the food production, pro- thally damaged.
tablishments are more significant ven- cessing and distribution systems have A few genera of foodborne bacteria
ues with respect to large, recognized changed the environment for foodborne (for example, Clostridium spp. and Bacil-
foodborne disease outbreaks. That is, pathogens. As the scientific understand- lus spp.) are capable of existing in two
single illnesses due to unsafe food han- ing of foodborne pathogens has become forms: active vegetative cells and dor-
dling at home are unlikely to be attrib- more sophisticated, so too have the con- mant spores. These two forms often dif-
uted to food and to be reported, even trol methods. These control efforts are fer in their resistance properties to heat,
though home food handling is an im- one of many driving forces in pathogen chemicals, irradiation and other environ-
portant cause of foodborne disease. evolution, and as such, their impact on mental stresses. Similarly, spores are
Poor handling practices are influenced the virulence and survival of foodborne typically more resistant than vegetative
by a large number of demographic fac- pathogens must be fully considered (Ar- cells to the alternative processing tech-
tors including age, gender, race, educa- cher, 1996). Scientists study the effect of nologies. Pasteurization inactivates vege-
tion and income (Beletshachew et al., processing technologies and other tative cells of disease-producing micro-
2000; Klontz et al., 1995). While target- changes to the microbial environment to organisms. To have a commercially ster-
ed food safety education programs have evaluate the effectiveness of control tech- ile product, however, the process must
reported some success, they are only nologies and also the potential that con- inactivate all microbial spores (usually
one component of a larger initiative to trol efforts will drive pathogen evolution. targeting spores of C. botulinum) that are
inform and motivate food handlers The many varied processes used to capable of germinating and growing in
about food safety (Meer and Misner, prepare and preserve the wide range of the food under normal storage condi-
2000; Yang et al., 2000). foods are frequently designed to inacti- tions.
Recent outbreaks of viral gastroen- vate, inhibit or prevent the growth of Differences in microbial resistance to
teritis illustrate some new discoveries pathogenic or spoilage microorganisms control methods may be found not only
regarding the significance of the food in the specific product. Any of these mi- between genera and species but also be-
handler in the initiation and propaga- croorganisms that survive the process tween strains of the same species. For
tion of outbreaks. Parashar et al. (1998) may be damaged. Consequently, process instance, at the genus level, some bacteri-
reported on the role of an asymptomat- evaluations and the microbial inactiva- al strains with unique resistance to ther-
ic food handler in a viral gastroenteritis tion kinetics on which they are based mal inactivation, irradiation, and high
outbreak associated with the consump- must consider sublethal injury of cells pressure processing have been identified,
tion of contaminated sandwiches. Re- and spores, as well as resuscitation of such as D. radiodurans and the thermo-
searchers discovered that NLVs could be cells and alternative germination path- plasmals, making it possible that, in the
shed in the feces for up to 10 days after ways of spores. These considerations future, a pathogenic “super bug” could
diarrhea ended in the food worker or by must be built into hazard analysis and emerge. Within species, some strains of
asymptomatic food handlers, and, risk assessment to adequately assess and common enteric pathogens such as E.
through poor personal hygiene, subse- control emerging food safety situations. coli and Salmonella are more resistant to
quently contaminate food. Green et al. the effects of low pH and high tempera-
(1999), in describing a prolonged viral ture than other strains of the same or-
gastroenteritis outbreak at a large hotel,
Resistance to Controls ganism. If a bacterial strain with resis-
noted that toilet rims (72%) and carpets The efficacy of a preservation tech- tance to multiple control technologies
(70%) had a high incidence of contami- nology is influenced by a number of mi- emerged, it could be a potential food
nation. These environmental surfaces croorganism-related factors that are gen- safety hazard that would be uncontrolla-
remained important reservoirs for the erally independent of the technology it- ble with technologies that have produced
propagation of the outbreak. In per- self. These factors include the type and safe products for generations. If the mi-
haps the most interesting study, Becker form of the target microorganism; the croorganisms proved to be pathogenic,
et al. (2000) reported a primary food- genus, species and strain of microorgan- the control process would have to be re-
borne NLV outbreak associated with the ism; its growth stage; selection by envi- designed to specifically inactivate it. Al-
consumption of boxed lunches that ronmental stresses; and sublethal injury. ternatively, if the “super bug” were not a
were served to a North Carolina college Among the foodborne microbiologi- pathogen or spoilage microorganism, it
football team. During a subsequent cal hazards, bacteria are generally the might be very useful as a possible surro-
game in Florida the next day, many primary targets for most preservation gate during process development and
members of the North Carolina team processes, and bacterial susceptibility to validation.
developed diarrhea and vomiting. sublethal cellular injury is of special Another factor that can affect bacte-
Twenty-four hours later, similar symp- concern. Processes designed to inacti- rial resistance to preservation processes
toms developed in some of the opposing vate pathogens also must address the re- is the stage of growth. Cells in exponen-
team members, illustrating the role of sistance properties in foods of other mi- tial or log phase of growth are generally
direct person-to-person transmission in croorganisms—such as viruses, yeasts, less resistant than cells in stationary


phase. The development of stress resis- ous exposure or through cross protec- many actions within the food processing
tance proteins in stationary phase is a tion triggered by environmental or pro- system—decontamination, sanitation,
contributing factor to this phenomenon. cessing factors including stresses such as and product formulation and preserva-
heat or acid (Davidson, 1999). Some re- tion—can injure cells that survive the
Selection by Environmental Stresses searchers have attempted to differentiate event (see Table 11).
various multiple stresses, e.g., lethal pH Some of these processes are classic
Extreme environments usually kill and water activity. Shadbolt et al. (2001) and well established as effective against
most bacterial cells and can result in the hypothesized that pH-induced stress pathogens that have existed in the past,
selection of mutant cells that are resis- causes an energy drain that sensitizes but new product formulations, new
tant to the severe conditions (see selec- the cell to other environmental con- equipment, or modified regimens can
tion, p. 21). Studies have suggested that straints. Similarly, the effect of habitual create opportunities for some microor-
bacterial stress may induce hypermuta- exposure to reduced water activity in- ganisms to survive, frequently in a suble-
bility, which would in turn lead to a mi- creased the heat tolerance of Salmonella thally injured state. New processes also
crobial population of greater resistance spp. (Mattick et al., 2000). Another ex- have the potential to create sublethally
(Buchanan, 1997a). Therefore, the expo- ample of cross protection is the in- injured pathogens.
sure of cells to some form of stress may creased radiation resistance caused by It would be a rare genus of bacteria
induce and allow the survival of micro- the induction of acid resistance in en- of concern in the food industry that has
organisms with unusually high durabili- terohemorrhagic E. coli (Buchanan et al., not in some situation demonstrated the
ty to a given inactivation process. 1999). capacity to be sublethally stressed or in-
The responses to stresses in the food Because environmental stress can jured by a food-related physical or chem-
system may play a major role in the emer- increase a pathogen’s resistance to con- ical insult. Many yeasts and molds asso-
gence of pathogens (Sheridan and Mc- trol technologies, the potential for in- ciated with food also have shown suscep-
Dowell, 1998). Bacteria are capable of creased resistance must be factored into tibility to sublethal damage. Early in the
adapting to an immediate environmental the process. The analysis should consid- study of cell injury, lactic acid bacteria
stress, but the response is temporary, and er: (1) if the food environments are like- used as starter cultures for dairy fermen-
the genes involved are switched off when ly to induce stress conditions in the mi- tations were shown to be cold-damaged,
the stress is removed (see stress, p. 22). croorganisms; (2) whether stress-in- requiring special nutrients for normal
The stress response may be triggered by a duced resistance could possibly occur at rapid growth.
single parameter or by several simulta- any point in the food processing opera- Sublethal injury may be demonstrat-
neously, causing variations in response. tion; and (3) if it did, whether it would ed or exhibited as more exacting require-
Some stress responses have particu- significantly impact the inactivation ments for growth, greater sensitivities to
lar relevance to the food processing envi- process and lead to possible underpro- antagonistic agents (e.g., selective agents
ronment. For example, stress responses cessing. Considering that most food in media or preservatives in a food), in-
to temperature shifts can affect L. mono- processing systems are designed to ex- creased resistance to subsequent inacti-
cytogenes attachment to food contact sur- pose microorganisms only once to any vation treatments by the same or differ-
faces (Smoot and Pierson, 1998). given stress-inducing factor (for exam- ent agents, increased lag time before ex-
The cross protective effect in which ple, heat, acid, or antimicrobials), a re- ponential growth ensues, or changed vir-
exposure to one stress triggers resistance sistant population is unlikely to develop. ulence as a pathogenic cell. The injured
to other stresses is a special concern in However, it is possible that sublethal in- cell may return to its initial native state
food processing environments. Mazotta jury to E. coli O157:H7 as it passes by repairing the cellular damage under
(1999) found that the heat resistance of through the low pH of a cow’s gas- suitable conditions. This resuscitation in
acid- or salt-adapted, heat-shocked, or trointestinal tract and then through an the absence of antagonistic agents or in
starved E. coli O157:H7 cells was higher acid rinse at slaughter may change its re- the presence of appropriate substrates
than that of cells grown to exponential sistance to heat inactivation during will result in a cell with its original capa-
or stationary phase under optimum con- preparation. Likewise, L. monocytogenes bilities, resistances, and virulence. In
ditions. To add an extra safety factor, cells in the production environment that other words, the damage of sublethal in-
Mazotta suggested using stress-inducing are sublethally injured by repeated ex- jury is reversible—it is not a permanent
culture conditions when studying the posure to sanitizers may have altered genetic change. This phenomenon is dif-
thermal resistance of vegetative patho- survival or virulence characteristics. An ferent from selection of a resistant mu-
gens in specific products. The cross pro- additional exception is previously pro- tant with a permanent genetic change.
tective effects of the bacterial stress re- cessed material that is reintroduced into The effectiveness of a microbial inacti-
sponse vary. Lou and Yousef (1997) de- the process stream. In this case, in- vation process is often measured by enu-
termined that sublethal stresses to etha- depth studies of the impact of process- merating any surviving organisms in a se-
nol, acid, hydrogen peroxide, heat, or salt ing-induced stress are needed. lective medium. Because viability in mi-
had variable effects on subsequent expo- croorganisms is generally based on the
sure of L. monocytogenes to normally le- Sublethal Injury ability to increase in numbers to some
thal levels of the same stressors. For ex- measurable level, death may be defined as
ample, heat shocking increased the resis- The microbial ecology of food is in- an irreversible loss of the ability to gener-
tance of the microorganism to ethanol, fluenced dramatically by food process- ate progeny (Mackey, 2000). Ideally, a mi-
hydrogen peroxide and salt, but not to ing and preservation technologies. croorganism exposed to processing con-
acid. Similarly, resistance to food antimi- Whether or not the actions are directly ditions would be either viable or dead; in
crobials can be acquired through previ- or indirectly aimed at microorganisms, actual practice, the control technology of-

Table 11. Conditions That Can Produce Sublethally lose their ability to 2001). Addition of 5% ethanol enhances
Injured Cells (Ray, 1989) grow in even nonselec- inactivation by organic acids and osmot-
tive environments that ic stress (Barker and Park, 2001). On the
Environmental Stress Processing Parameter normally support their other hand, cross protection from micro-
growth but are consid- bial stress responses must be considered
Moderate heat Pasteurization ered still viable be- when evaluating treatment effectiveness.
Concentration cause the cells remain Growth under low aw conditions increas-
Low temperature Refrigeration/chilling physically intact and es the heat resistance of Salmonella spp.
Freezing demonstrate metabol- (Mattick et al., 2000). Combined ap-
ic activity. The VBNC proaches are not new, nor are they limit-
Low water activity Dehydration state of microbial cells ed to vegetative cells. Apparent inactiva-
High solutes (salt, sugar) has been reported to tion and control of heat-damaged C. bot-
Radiation X-rays occur in a number of ulinum spores was considerably less in
Gamma rays foodborne pathogens food that contained lysozyme (Peck and
Ultraviolet rays as an outcome of envi- Fernandez, 1995).
ronmental stress As scientists continue to improve
Low pH Organic or inorganic acids (McKay, 1992; Xu et their understanding of microbial stress
al., 1982). The possi- responses, it is increasingly possible to
Preservatives Sorbate
bility exists that these try to anticipate potential stress-related
VBNC cells, which are problems in the food processing envi-
Sanitizers Chlorine non-detectable by tra- ronment. The food industry is adopting
Quaternary ammonium compounds ditional cultural meth- or considering a variety of methods for
Short-chain fatty acids ods, may cause disease sanitizing beef, pork, lamb, and poultry
Peroxyacetic acid if consumed (Colwell carcasses and reducing or eliminating
et al., 1985). If they are pathogens in meat products (Mermel-
Pressure High hydrostatic pressure
developed in a food stein, 2001). Whether it is steam pas-
Electric fields Pulsed electric fields production environ- teurization, rinsing with various anti-
ment, a food safety microbials, e-beam or x-ray treatment,
Nutrient deficiencies Very clean surfaces risk may be presented. high pressure processing, or some yet to
The very existence of be identified procedure, it is essential
the VBNC state has that the stress-induced responses be
ten produces a continuum of effects in- been questioned, based on studying the considered.
cluding some degree of cellular injury. concept from alternative perspectives The same considerations are essential
Injured cells can be easily underesti- (Bloomfield et al., 1998; McDougald et al., for the decontamination procedures used
mated, resulting in misleading conclu- 1998). New approaches to studying the with fresh and fresh-cut fruits and vegeta-
sions about the efficiency of the inactiva- VBNC phenomenon need to be taken, to bles. High pressure processing of orange
tion method. If the cell damage is not arrive at an agreement regarding its oc- juice (Zook et al., 1999), pulsed electric
recognized, the loss of specific identifi- currence, and then to determine if these field treatment of orange-carrot juice
able characteristics as a result of suble- microorganisms have any importance in (Rodrigo et al., 2001), UVB treatment of
thal injury leads to faulty data. Injury the food production environment and to surface waters (Obiri-Danso et al., 2001),
occurs in vegetative cells and bacterial food safety and the public health. sanitizer treatment of Salmonella attached
endospores of pathogenic and non- to apples (Liao and Sapers, 2000), and
pathogenic microorganisms. A cell that Future Implications disinfectants killing Alicyclobacillus aci-
appears to be “dead” because it is unable doterrestris spores prior to pasteurizing
to multiply and demonstrate its viability The responses to stresses in the food fruit juices (Orr and Beuchat, 2000) are
may be able to repair itself under some system may play a major role in the only a few examples of possibilities for the
special circumstances. So a food, pro- emergence of pathogens (Sheridan and future. If sublethal injury were to be ig-
cess, or other microbial environment McDowell, 1998). Stress responses may nored in these very promising food safety
could appear to be pathogen-free only to increase the pathogen’s resistance to in- developments, new food safety problems
become dangerous when the injured cells activation methods, improve its ability to may occur. These concerns also apply to
recover. Mackey (2000) has described the survive in the food processing environ- multiple or combination processes that
nature of sublethal injury, emphasizing ment, and enhance its ability to cause ill- are intended to benefit from additive or
the many conditions that influence inju- ness when consumed by humans. synergistic effects. For example, pulsed
ry, resuscitation, and recovery, and high- Scientists are studying the response high pressure processing with modest ele-
lighting the role that sublethal injury of cells and spores to multiple stress vated temperatures appears to inactivate
may play in the design of preservation treatments in an attempt to develop new spores with high heat resistance (Meyer et
processes. and better control systems for specific al., 2000).
Another irregular or unnatural state situations. Combined treatment meth-
or condition that microorganisms may ods take advantage of stress-induced mi- New Tools for Pathogen Research
enter is the viable (or metabolically active) crobial weaknesses. For example, pres-
but nonculturable (VBNC) condition in sure-damaged E. coli are more sensitive New tools are needed to more easily
response to stress. These microorganisms to acid than native cells (Pagan et al., and specifically monitor populations of


pathogens in the post-harvest stages of low for the recovery of many of the in- may be present. Conventional methods
food production. Although much of the jured cells (see sublethal injury, p. 63). for determining microbiological injury
emphasis in microbiological methods In direct plating, the sample is placed generally involve plating on two types
development traditionally has been on directly on or in selective media, which of media, i.e., selective and non-selec-
pathogen detection in the food, it is crit- may inhibit the growth of the injured tive; the rationale being that injured
ical to develop better ways of monitor- cells. The MPN technique, however, is cells cannot survive selective culture
ing the food processing environment, so extremely labor intensive. Molecular and can grow only on non-selective
that the factors that influence food con- techniques, such as the coupling of im- media, whereas healthy cells can grow
tamination may be understood. This munochemical or nucleic acid-based on both types of media (Ray, 1979).
understanding is a necessary step in the assays to the MPN, or nucleic acid This strategy is somewhat imprecise;
development of rational control strate- probe hybridizations of colony blots (de with each additional selective agent in-
gies. Blackburn and McCarthy, 2000; FDA, corporated into the medium, greater
Traditional identification methods 1998; Miwa et al., 1998), are increasing- percentages of injury in the population
based on microbiological culture are ly being applied to traditional methods can be revealed, indicating the presence
time-consuming, prohibiting scientists for obtaining results more quickly. of different subpopulations of cells
from accumulating the large amounts PCR, originally developed for screen- having varying degrees or different
of data needed to develop an under- ing/detection applications, has been types of injury. Molecular methods of
standing of the ecology of pathogens in modified for use as a quantitative assay analysis, in addition to those based on
the food production environment. The (Nogva et al., 2000). Recombinant bi- culture, can provide useful insights for
commercial market has provided no oluminescent strains of food pathogens assessment of injury and viability of
shortage of rapid method “kits,” which have been used to quantitatively assess pathogen cells. Molecular probes of
employ either immunochemical or nu- survival in foods and the food process- cellular functions, e.g. membrane per-
cleic acid-based detection technology, ing environment by measurement of meability, respiratory electron trans-
but they are expensive and must be light emission (Ramsaran, et al., 1998; port, membrane esterase activity, etc.,
validated for each particular applica- Siragusa et al., 1999). These techniques may be useful for broadly categorizing
tion. and others need to be further developed, types of cellular injury (Breeuwer and
Research on biofilms, a persistent refined and validated as our need for Abee, 2000; McFeters et al., 1995; Porter
problem in the food plant environment quantitative information on pathogens et al., 1995). Expression assays that
(Wong, 1998), is slow because the increases. build on technologies such as the re-
unique methods and instrumentation The development of genetic finger- verse transcription (RT)-PCR (Sheri-
needed for their study are not widely printing techniques has provided the dan et al., 1998), the nucleic acid se-
available (Zottola, 1997), and because ability to finely discriminate strains quence-based amplification (Blais et
food microbiologists generally have not within a species of pathogen. Several al., 1997; Simpkins et al., 2000), and
been trained in these techniques. Bio- variations of fingerprinting techniques use of reporter gene constructs (Cha et
films are a growing colony or mass of are available (Farber et al., 2001), and al., 1999; Stewart et al., 1997) may be
bacterial cells, attached to each other new ones continue to be developed. Ge- useful for studying the expression of
and a surface, that entrap debris, nutri- netic fingerprinting has been extremely genes known to be associated with
ents, and other microorganisms (Zotto- useful in epidemiological work and stress. However, because we do not
la, 1994). To research such issues, food identification of foodborne illness out- know what all of these genes may be,
microbiologists must adopt more tools breaks (e.g., PulseNet) (CDC, 1999d). the development of new tools, such as
that are traditionally the province of the The technology has begun to be applied genomic microarrays (Graves, 1999)
microbial ecologist. to the study of pathogens in the food for food pathogens, is needed. A ge-
Although many traditional culture plant environment (Norton et al., 2001). nomic microarray or “gene chip” could
methods are available and many rapid This novel approach allows questions be, for example, an ordered set of all of
methods have been commercialized for about pathogen evolution, persistence the known genes of a particular micro-
screening/detection of foodborne and routes of contamination in the food organism, deposited in precise loca-
pathogens (FDA, 1998), the options are plant to be examined. tions on a small solid surface. A prom-
much more limited if a quantitative de- New tools also need to be developed ising use for genomic microarrays is in
termination is desired. Sensitive quanti- and applied for assessing stress and in- expression analysis, in which changes
tative methods are necessary for assess- jury of pathogens in the food produc- in the pattern of expression of thou-
ing pathogen growth, survival and inac- tion environment. Sublethally injured sands of genes can be studied simulta-
tivation, as well as for accurate risk as- cells may have different survival char- neously, known as “functional genom-
sessment. Specific quantitative determi- acteristics during food storage or after ics” (Oh and Liao, 2000; Tao et al.,
nations are traditionally obtained by the consumption, and may show greater re- 1999). Studying the effect of a particu-
most probable number (MPN) tech- sistance to control measures and lar stress on a pathogen, then, no long-
nique, a sample dilution technique for heightened virulence than the original er needs be limited to expression of one
statistically estimating the number of population (Abee and Wouters, 1999; or a few stress response genes. Func-
microorganisms, or if background pop- Bower and Daeschel, 1999; Gahan and tional genomics will become
ulations are not too intrusive, by direct Hill, 1999). If the injured cells are not an invaluable tool for understanding
plating (FDA, 1998). The MPN tech- detectable by the method chosen, the and monitoring stress responses in
nique is the most sensitive, because it safety of a food process may be as- the food production and processing
provides enrichment conditions that al- sumed, when, in fact, a food safety risk environment.

Ability of Pathogens
To Survive in the
Environment lated from five of 25 surface samples of time the cheeses were turned daily
Vacherin Mont d’Or, a soft smear-ripened and brushed with salt water. Once
The Vaudois University Hospi- cheese manufactured from October to ripened, they were packaged and
tal Medical Center in Lausanne, March and consumed primarily in the returned to the cheese factory. To
Switzerland, generally diagnoses a outbreak region. Furthermore, all five validate suspicions that the con-
mean of three listeriosis cases per isolates belonged to serotype 4b, and tamination occurred during ripen-
year. However, a cluster of 25 liste- two of the phage types isolated from the ing, investigators took samples
riosis cases (14 adults and 11 ma- cheese were identical to most clinical from the wooden shelves, brushes
ternal/fetal) was observed at the strains isolated during the 1983-1986 and the surface rind of the cheese.
same medical facility between Janu- epidemic period. Analysis of these samples revealed
ary 1983 and March 1984, with 15 In 1987, a third case-control study fairly high levels of L. monocytoge-
additional cases diagnosed at sur- demonstrated that 31 of 37 individuals nes (10,000 to 1,000,000 bacteria).
rounding hospitals (Bille, 1988; Ma- who became ill had consumed Vach- Further investigation showed that
linverni et al., 1986). erin Mont d’Or cheese, as compared almost half of the 12 ripening cel-
with only 20 of 51 people in the con- lars were contaminated with one or
Epidemiology trol group. Investigators isolated the both epidemic strains of L. mono-
epidemic strain of L. monocytogenes cytogenes, suggesting cellar-to-cel-
This epidemic appeared atypi- from a piece of Vacherin Mont d’Or lar spread of the pathogen, which
cal because of the high number of cheese that had been partially con- would explain why cheeses in all 40
healthy, immunocompetent indi- sumed by one of the victims. There- plants were contaminated. Al-
viduals affected, the high rate of fore, Swiss officials halted production though first detected in 1983, inves-
brain-stem encephalitis, and a of the cheese and recalled the product tigators speculated that the outbreak
mortality rate of 45%. The organ- throughout Switzerland. Between 1983 began several years earlier, based on
isms isolated from clinical speci- and 1987, a total of 122 cases of listeri- evidence that the epidemic strain
mens from thirty-eight of the 40 osis resulting in 34 deaths were record- had been isolated from a listeriosis
patients involved in the outbreak ed in the western part of Switzerland. victim in 1977. Thus, this particular
were serotype 4b. A high number Several years following the out- strain of L. monocytogenes had es-
(92%) of the L. monocytogenes se- break, the isolates were further typed tablished itself and survived in the
rotype 4b cultures were of two using a variety of new methods, and factories and/or cellars of various
unique phage types, compared the clinical and cheese isolates were plants for up to 10 years.
with only 44% of the serotype 4b identical. The epidemic strain had the All 40 factories and 12 cellars
cultures obtained during the pre- same phage type, enzyme type, ri- were thoroughly cleaned and sani-
vious 6 years. This evidence indi- botype and PFGE type as strains iso- tized. The wood from the ripening
cated the outbreak might be traced lated during the 1985 listeriosis out- cellars was removed and burned,
to a single source. A thorough break in California. and the cellars were refitted with
case study did not identify the metal shelves. Examination of ex-
source or mode of Listeria trans- Management perimental batches of the cheese
mission, however, public health of- produced over a 2-month period
ficials initiated a prospective case- Immediately following the recall, indicated the cleanup effort was
control study, assuming that a Swiss officials began investigating how successful.
similar listeriosis outbreak was the cheese could have become contami- It is evident that L. monocytoge-
likely the following winter. Over- nated. The cheese implicated in this nes can adapt to different plant
all, 16 additional cases were identi- outbreak was produced at 40 different conditions and persist in the man-
fied between November 1984 and factories located in western Switzerland, ufacturing environment for
April 1985. and all contaminated cheese was report- months and even years. From these
After a 1985 listeriosis outbreak edly prepared from Listeria-free bovine environmental niches/biofilms, the
in California was linked to con- milk. After coagulating the milk, the re- organism can find its way into fin-
sumption of Mexican-style cheese, sulting curd was dipped into wooden ished product, and cause sporadic
Swiss officials initiated a baseline hoops and allowed to drain for 1-2 cases or outbreaks of foodborne
study to detect Listeria spp. in a va- days. When drained, the cheese was listeriosis. As a part of an overall
riety of dairy products. While sur- transported to one of 12 cellars located control strategy, aggressive envi-
veying soft, semi-hard, and hard throughout the area and ripened for 3 ronmental and product monitoring
cheeses, L. monocytogenes was iso- weeks on wooden shelves, during which is needed.


Application of Science to
Food Safety Management
Effective application of our current ence-based policies for food safety and ensuring that countries establish food
scientific knowledge is a vital part of public health protection is risk analysis. safety requirements that are scientifi-
Risk analysis is generally considered to cally sound and by providing a means
continuing efforts to improve food have three components: risk assessment, for determining equivalent levels of
safety. Our food safety policies are risk management, and risk communica- public health protection between
tion. New scientific tools can provide countries. Without systematic risk as-
based on the best scientific informa-
ways to assess risk, enabling decisions to sessment, countries could set require-
tion available at the time they were be based on data and fact. These deci- ments unrelated to food safety, creat-
created, but our knowledge continues sions are not easy, but risk assessment ing artificial barriers to trade. Recog-
gives us the basis for managing these nizing the importance of this science-
to improve. Flexible, science-based risks in an informed, intelligent way. An based approach to fair trade, the
policies should incorporate new effective food safety system integrates World Trade Organization requires
science and risk analysis at all levels of each country’s food safety measures to
information as it becomes available.
the system, including food safety re- be based on risk assessment. The Co-
Everyone benefits from science-based search, information and technology dex Alimentarius Commission (Co-
policies, although factors such as transfer, and consumer education. dex), which establishes international
food safety standards, has developed
economic impact and other trade-offs
Risk Assessment principles and guidelines for conduct-
are part of the policy-making environ- ing risk assessments (CAC, 1999).
ment as well. Ideally, food policy will Broadly defined, risk assessment is Regardless of the specific format, a
the use of scientific data to identify, char- risk assessment has four main compo-
draw on a variety of science-based tools acterize, and measure hazards; assess ex- nents:
and be structured to provide the posure; and characterize the risks in- • Hazard identification involves identi-
volved with a food. However, risk assess- fying the hazard (e.g., pathogen), the na-
flexibility to apply these tools as
ments do not specifically determine ture of the hazard, known or potential
science dictates. whether a product is “safe” or “unsafe.” health effects associated with the hazard,
The final decades of the twentieth In terms of foodborne illness, risk is and the individuals at risk from the haz-
century saw tremendous change in our a function of the probability of an ad- ard.
knowledge of pathogenic microorgan- verse health effect and the severity of that • Exposure assessment describes the
isms, their toxins and their metabolites. effect. In other words, risk is a measure exposure pathways and considers the
Scientists identified a wide array of mi- of the likelihood that illness will occur likely frequency and level of intake of
crobial hazards, and foods previously within a population as a result of a haz- food contaminated with the hazard.
thought to be safe were found to be im- ard in food and the severity of that ill- • Hazard characterization explores the
portant vehicles of foodborne disease. ness (Buchanan, 1997b). relationship between the exposure level
This new knowledge resulted in new When used in food safety regulation and the nature of the adverse effects,
policies to protect consumers. This sce- or policy development, risk assessment considering both frequency and severity.
nario will continue into the new centu- reflects the expected impact of a particu- • Risk characterization identifies the
ry. lar food safety problem, the expected im- likelihood that a population of individu-
Unfortunately, current systems can- pact of protective mitigation measures, als would experience an adverse health
not deliver a risk-free food supply. The and the levels of urgency and controver- outcome from exposure to the food that
scientific knowledge, technology and sy surrounding an issue. Risk assess- might contain the pathogen. The risk
equipment are not available to eliminate ment has long been applied to assessing characterization also describes the vari-
all microbial hazards from all foods. risks associated with chemical exposure ability and uncertainty of the risk and
This vulnerability will continue to in- but only recently has it been formally ap- identifies data gaps in the assessment.
fluence regulatory policy as regulatory plied to foodborne pathogens. There- These same four components are
agencies and industry seek solutions to fore, a specific format for these risk as- considered in both quantitative and
these hazards. The primary weakness in sessments is still in the definition pro- qualitative risk assessments. Qualitative
today’s control system is the presence of cess; currently used formats vary de- risk assessments may be chosen to iden-
enteric pathogens on raw agricultural pending upon the scope and objective of tify, describe, and rank hazards associat-
commodities (e.g., meat, poultry, milk, the assessment. ed with a food. Quantitative risk assess-
eggs, fruits, vegetables, and seafood). Risk assessments also play an im- ments may be chosen when substantive
As a result, an essential part of sci- portant role in international trade by scientific data are available for analysis,

and these risk assessments almost always of qualitative risk assessments, they are frequently done to model the many cir-
yield a numerical expression of risk. frequently used and serve a purpose in cumstances that may surround expo-
science-based food safety management. sure. And since foodborne pathogen
Qualitative Risk Assessment Qualitative risk assessment will continue growth, inactivation and survival are
to play a role in the future when time highly dependent upon intrinsic (food-
Qualitative risk assessment is gener- and money constraints prohibit a full related) and extrinsic (environmental)
ally considered a valuable method to de- quantitative risk assessment. However, factors such as relative humidity and
termine which hazards are associated scientists must develop a better under- storage temperature, mathematical
with a particular food. This process is of- standing of the exact role that qualitative models such as USDA’s Pathogen Mod-
ten used by an expert panel. Also, quali- risk assessments can play and a better eling Program can be used to estimate
tative assessments are useful when many overall defined structure for these risk the effect of these factors on microbial
gaps in the available data limit the preci- assessments. persistence and levels in foods.
sion necessary for a quantitative risk as- The relationship between the inges-
sessment. For instance, scientists often Quantitative Risk Assessment tion of pathogenic microorganisms and
have little exact information about the possible health effects may be described
relationship between the quantity of Quantitative risk assessment is for- as the quantitative relationship between
pathogen ingested and resulting frequen- mally defined as the technical assessment the intensity of exposure (dose) and the
cy and severity of adverse health effects, of the nature and magnitude of a risk frequency of the occurrence of illness
especially for susceptible subpopula- caused by a hazard. The technique, first within the exposed population of hosts
tions. Information about exposure—the developed in the 1950s to evaluate nuclear (response). For pathogenic microor-
probability of contamination, the extent proliferation risks, has since been used to ganisms, this is dependent upon the
of pathogen growth in the food, and the evaluate the toxicological risks to plants, number of units of infectious agent in-
amount of the food consumed by vari- animals, and public health posed by gested in the food, the infectivity and
ous populations—is sometimes limited. chemical exposure and more recently in pathogenicity of the infectious agent,
Qualitative risk assessments can be use- microbiological food safety evaluation. and the vulnerability of the host. The
ful in identifying these data gaps and in As the name implies, quantitative risk purpose of the hazard characterization
targeting or prioritizing research that assessment ultimately provides numerical step is to quantify or statistically de-
would have the greatest public health im- estimates of risk that can be used in regu- scribe the relationship between the risk
pact. latory decision-making and risk manage- agent and the magnitude of the adverse
Qualitative risk assessments have nu- ment. Quantitative microbial risk assess- effect. Included in this step is a full de-
merous applications in food safety anal- ment as a discipline has been under scru- scription of the severity and duration of
ysis. These assessments can help compa- tiny recently, purportedly because of a adverse effects that may result from the
nies develop more effective Hazard Anal- lack of rigor and precision. Because the ingestion of a microorganism or toxin
ysis Critical Control Points (HACCP) process inherently depends upon the in- in a food. The source of data used for
plans based on scientific data. For in- put of many scientists from frequently di- hazard characterization is usually hu-
stance, a qualitative risk assessment can verse disciplines, as well as the incorpora- man challenge studies, whereby a de-
help identify likely hazards, although the tion of assumptions when definitive data fined population of consenting adults is
result might only be to rank a hazard as are lacking, some individuals believe that given various doses of the infectious
high, medium, or low in terms of preva- the process is little more than an academic agent, and their response is measured as
lence or potential contamination level. exercise. Of all the limitations in the cur- infection or disease. For pathogens
The assessment will have an increased rent risk assessment methodology causing mild disease, this is feasible; for
power to inform decision-makers when (Jaykus, 1996), the need for more and bet- those associated with more severe dis-
the risk of an adverse health effect can ter data is the most pressing. eases, or affecting particularly suscepti-
also be described, at least qualitatively as After the hazard identification phase ble populations, risk assessors must rely
high, medium or low. is complete, the exposure assessment es- on animal models of disease or other
A significant disadvantage of qualita- timates or directly measures the quanti- data sources. The raw input data from
tive risk assessments is the inability to ties or concentrations of risk agents re- these types of studies is used in con-
compare the extent to which particular ceived by individuals or populations. junction with statistical methods that
mitigating factors or risk management As such, exposure assessment is de- describe the dose-response relationship
options can successfully reduce risk. A signed to characterize the circumstanc- in mathematical terms. Some frequent-
qualitative risk assessment can compare es, source, magnitude, and duration of ly used dose-response models include
two options that both address the expo- exposure, the final goal of which is to the Beta-Poisson, Exponential, and
sure to a hazard—e.g., two different dis- produce a mathematical expression for Gamma-Weibull models.
infecting agents—or it can compare two exposure, generally in the form of the Risk characterization is the final step
options that address the effect—e.g., two probability of ingestion of the infec- of risk assessment and represents the inte-
methods to prevent susceptible individu- tious agent through the food vehicle of gration of the exposure assessment and
als from consuming the food. However, interest. Common data sources include hazard characterization to obtain a risk
qualitative risk assessments present diffi- survey information on the prevalence estimate of the likelihood and severity of
culties when trying to compare one op- and levels of contamination for a par- the adverse effects that would occur in a
tion that addresses only exposure and ticular pathogen in a particular food given population. The final risk estimate
another option that addresses only effect. commodity. Scenario analysis using should incorporate information about the
Notwithstanding the disadvantages various computer software packages is variability, uncertainty and assumptions


identified in all previous steps of the risk models are properly constructed, they use. Often, the panel uses a process that
assessment. Statistical methods are used can be readily updated as additional in- is very similar to a HACCP hazard analy-
to characterize variability associated with formation becomes available. sis. In some instances, a rough estima-
a well-characterized phenomenon, while tion of the risks associated with different
Monte Carlo and Bayesian approaches Role of Expert Panels likely scenarios is sufficient. One ap-
can be applied in an effort to better char- proach is to assign relative probability
acterize uncertainty associated with a The process used by expert panels is and impact rankings—such as negligible,
poorly characterized phenomenon. Sen- very similar to that for qualitative risk as- low, medium, or high—to the likelihood
sitivity analysis is frequently done to bet- sessment. The major difference is that ex- of exposure and adverse outcome. The
ter understand the contribution of the in- pert panels, in general, collect and review panel must clearly define and justify the
dividual factors that influence the overall available information and develop guid- rankings to enable people to use the final
risk estimate. Because the risk assessment ance or recommendations for use by result without misinterpretation.
process usually involves extensive data in- government and/or industry. Thus, spe- An expert panel considers various
put, the use of various mathematical cific risk management options are an ex- aspects of the issue and provides its best
modeling approaches, and some degree of pected outcome from the expert panel judgment based on information avail-
assumption on the part of the assessors, process. In addition, the time frame for able at that time. Because the process is
risk assessment teams now seek to pro- an expert panel would normally be in simpler, it is also faster than a quantita-
vide “transparent” documents that give days or perhaps several months, the ex- tive risk assessment. Although the com-
the reader a full and detailed description tended time being used to prepare the re- plexity of the risk evaluation may vary,
of the process. port of the panel’s deliberations and rec- the panel follows the standard four-step
At present, the first reports of micro- ommendations. format for a risk assessment and should
bial risk assessment in food safety have Expert panels can effectively gather provide information on the conditions
appeared in the scientific literature, and information, evaluate available data, that lead to hazardous food. In the end,
several regulatory agency-driven risk as- and develop recommendations in a rel- the panel may recommend one or more
sessments have been completed in the atively short period of time. Expert pan- measures to control a hazard or, if neces-
United States during the last 5 years: the els can be used to address a variety of sary, the expert panel may recommend
USDA/FDA Salmonella Enteritidis risk circumstances: when a rapid decision is banning the product or process. An ex-
assessment for shell eggs and egg prod- needed to address a newly recognized pert panel also may recommend estab-
ucts (USDA/FSIS, 1998a); the USDA/ concern, when resources and/or data lishing a Food Safety Objective when it
FSIS risk assessment for Escherichia coli for a quantitative risk assessment are would be an effective means to enhance
O157:H7 in beef and ground beef limited, or when few management op- the safety of the food under consider-
(USDA/FSIS, 1998b); the FDA draft as- tions exist. When epidemiological evi- ation.
sessment of the relative risk to public dence indicates a hazard is not under
health from foodborne Listeria monocy- control, panels may identify ways to in- Risk Management Using Food
togenes among selected categories of crease consumer protection. Also, pan- Safety Objectives
ready-to-eat (RTE) foods (FDA/CFSAN, els may address concerns raised by
USDA/FSIS, and CDC, 2001); and the changes in food processing technolo- A recently proposed risk manage-
FDA draft assessment on the public gies, food packaging, or distribution ment approach revolves around the con-
health impact of Vibrio parahaemolyticus systems. Expert panels can address cept of Food Safety Objectives (FSOs).
in raw molluscan shellfish (FDA/CF- such situations and evaluate the risk, As defined by the International Commis-
SAN, 2001). Other risk assessments have based on scientific evidence. sion on Microbiological Specifications
been completed by the Canadian Food Government and international bod- for Foods (ICMSF, 1997, 2002), a food
Inspection Agency. Despite these very ies have made extensive use of expert safety objective (FSO) is a statement of
significant efforts, the application of panels (e.g., Food and Agriculture Orga- the maximum frequency and/or concen-
quantitative risk assessment techniques nization of the United Nations (FAO)/ tration of a microbiological hazard in a
to microbiological foodborne hazards is World Health Organization (WHO) food at the time of consumption that
still in its relative infancy. consultations) to address concerns provides the appropriate level of protec-
Quantitative risk assessment pro- about the safety of a particular hazard- tion. The FSO approach can be used to
vides a formal, conceptual framework for food combination. In addition, industry integrate risk assessment and current
the evaluation of foodborne disease expert panels have considered the fac- hazard management practices into a
risks, one that effectively uses all avail- tors leading to foodborne disease and framework that can be used to achieve
able information and expertise. Prior to developed recommendations for their public health goals in a science-based,
the advent of this discipline, decisions control (e.g., the Blue Ribbon Task flexible manner. Fig. 7 demonstrates how
about food safety regulation and man- Force established by the National Live- the FSO concept (boxes with rounded
agement were much less systematic. Fur- stock and Meat Board to address E. coli corners) can integrate with HACCP
thermore, recent risk assessments pro- O157:H7) (NLSMB, 1994). (shaded boxes).
vide a clear picture of the role of uncer- Expert panels rely on epidemiolo- Although the FSO concept is relative-
tainty in overall risk modeling, using gists, public health specialists, food mi- ly new and is still evolving, its acceptance
some of the more robust methods, such crobiologists, food technologists and is growing because it offers a practical
as Monte Carlo simulation, to character- others with knowledge about the food- means to convert public health goals into
ize uncertainty. Finally, risk assessment borne disease or the conditions of food values or targets that can be used by reg-
is, by nature, an iterative process; if the production, processing, distribution and ulatory agencies and industry. For exam-

Fig. 7. Framework for
Public health concern identified
Food Safety Management
Risk Assessment

Hazard(s) identified

Exposure assessed

Hazard(s) characterized

Risk characterized
FSO Approach Risk Management

Consider options, including a Food Safety Objective

Hazard Control and Monitoring

Agricultural interventions implemented

GMPs/GHPs implemented

Baseline level of microbial hazard measured

Processing safety objective calculated

(FSO minus growth during storage and distribution)

Performance criteria established

(baseline minus processing safety objective)

Method(s) of control selected Process-specific hazard analysis conducted

Critical control points identified

Process/product criteria established

Critical limits established

Monitoring procedures developed and implemented

Corrective actions implemented (as needed)

HACCP system verified

Recordkeeping implemented

Microbiological criteria established (if necessary)

Processing safety objective met

Food Distribution and Storage

Pathogen growth prevented or minimized

Food Consumption

Food Safety Objective met


ple, a public health goal may be to reduce safety objectives to communicate the emerging food safety concerns, there
the incidence of foodborne illness attrib- level of control expected in food pro- may be little information available. It is
uted to pathogen A by 50% from 20 to 10 cesses and then to evaluate the adequa- the responsibility of regulatory agencies
cases per 100,000 people per year. A reg- cy of a facility’s control system. to establish criteria that can be used to
ulatory agency or manufacturer cannot FSOs differ from the microbiologi- assess the safety of foods. Preferably, the
design control systems that would be cal criteria that have been traditionally criteria should be considered interim
certain to meet such a goal. However, if used to determine the acceptance of standards that will be adjusted to be
this goal were translated into a numeri- food products. Microbiological criteria more or less stringent as more informa-
cal measure of the microbiological haz- specify details such as a sampling plan tion becomes available.
ard’s frequency or concentration (e.g., and the method of sample preparation The FSO approach assumes that a
less than 100 CFU/g of L. monocytoge- and analysis, but the criteria cannot be food is distributed, stored, and prepared
nes or less than 15 mg/kg of aflatoxin), readily used to evaluate a process. Mi- as intended and expected when the food
then the regulatory agency could estab- crobiological testing of finished product safety system was designed. Deviations in
lish inspection procedures and industry from a plant provides a snapshot for the handling and storage after the food
could design control processes based on time the food was produced. Review of meets the processing safety objective at
the FSO. the same plant’s food safety manage- the factory could trigger a failure to meet
The FSO concept can be a useful ment system using an FSO approach the FSO. Proper food handling and
tool for creating policies that are consis- would provide a more meaningful as- preparation practices are essential under
tent with current science. The limits im- sessment of long-term control. the FSO approach.
posed in an FSO should reflect not only FSOs can be used to communicate
the best available scientific information food safety requirements for food pro- Hazard Control and Monitoring
but also nonscientific input from a vari- cesses; whereas microbiological criteria
ety of sources. FSOs should reflect soci- are used to determine the acceptability Once an FSO has translated public
etal values with regard to levels of con- of specific lots of food with respect to health goals into quantifiable limits, haz-
sumer protection. The FSO develop- quality and/or safety. The principles for ard control and monitoring practices
ment process should be transparent and the establishment of microbiological must be developed. Although hazard
facilitate input, both scientific and soci- criteria for food have been described by controls were developed long before the
etal, from all affected parties. Codex (CAC, 1997a) and have been re- more recent formal risk assessment and
The FSO approach integrates scien- cently further elaborated upon by the risk management approaches, the appli-
tific data from risk assessment to set ICMSF (ICMSF, 2002). For example, the cation of hazard controls can be directed
quantifiable standards that address spe- following components are recommend- and informed by the broader perspective
cific public health outcomes. Because ed when microbiological criteria are to that results from an integrated food safe-
the FSO must be met at the time of con- be established: ty framework. Mandatory hazard con-
sumption, it is necessary to consider the • a statement of the microorganisms trol processes have traditionally been the
potential for pathogen growth during of concern and/or their toxins/metabo- focus of regulatory agencies, but recent
storage and distribution. The processing lites and the reason for that concern; initiatives to develop risk-based ap-
safety objective is the FSO minus any • microbiological limits considered proaches offer the opportunity for flexi-
projected pathogen growth. For exam- appropriate to the food at the specified ble, science-based hazard control.
ple, if the FSO is less than 100 CFU/g of point(s) of the food chain, Often, many different approaches
L. monocytogenes and 1 log cycle of • the number of analytical units that are combined to achieve the desired re-
growth is projected, the processing safe- should conform to these limits; sult. In the farm-to-table approach to
ty objective is calculated as no more • a sampling plan defining the number food safety, good agricultural practices
than 10 CFU/g of L. monocytogenes. If of field samples to be taken, the method (GAPs) can provide ingredients with
no pathogen growth is projected, the of sampling and handling, and the size of improved microbiological safety. GMPs,
processing safety objective is the same the analytical unit; and also known as GHPs in the internation-
as the FSO. • the analytical methods for their de- al arena, set basic standards for facility
The processing safety objective is tection and/or quantification. sanitation and hazard control. Perfor-
then used to develop the performance In addition, a microbiological criteri- mance criteria quantify the hazard con-
and process/product criteria and to es- on should also state: trol results necessary to meet the pro-
tablish verification and acceptance • the food to which the criterion ap- cessing safety objective, and process/
procedures. Good hygienic practices plies; product criteria define the process vari-
(GHPs) and good manufacturing prac- • the point(s) in the food chain where ables and product characteristics that
tices (GMPs) are important to mini- the criterion applies; and will achieve the performance criteria.
mize the hazard and prevent recontam- • any actions to be taken when the cri- HACCP establishes the critical control
ination after processing. HACCP man- terion is not met. points at which the process/product cri-
ages the application of control meth- When used for food safety, microbi- teria are applied, further defining the
ods, ensuring that the process is effec- ological criteria should reflect the sever- conditions that must be met into a spe-
tive. Table 12 provides three examples ity of the disease and whether risk is cific set of critical limits for the process.
of how the FSO approach might be likely to decrease, remain the same, or HACCP also monitors and documents
used to address specific issues of mi- increase between when a food is sam- successful implementation of the con-
crobiological food safety. Regulatory pled and when it is consumed. As crite- trol process. Finally, microbiological
agencies can use FSOs and processing ria are established to address newly criteria and testing may be used, if nec-

Table 12. FSOs in the Food Safety Management Framework (Derived from ICMSF, 2002)

Managing Microbiological Food Safety Salmonella in Dried Milk

Public health concern Consumed as reconstituted milk, particularly by children

(often based on epidemiological data)

Risk Assessment
Hazard identification Salmonella are heat-sensitive bacteria that are a leading cause of
diarrheal disease worldwide, especially among the very young and
Exposure assessment Post-processing contamination in the factory rarely occurs, and the
concentration of Salmonella in dried milk is low

Hazard characterization Considering reconstituted dried milk is often consumed by children,

assume worst case scenario: one Salmonella cell per 10 g serving of
milk may cause illness
Risk characterization Based on limited data, probability of illness is <1 in 108 servings

Risk Management
Food safety objective To maintain the current estimated level of risk, FSO may be established
as <1 Salmonella per 108 gram at the time the dried milk is reconsti-
tuted for consumption

Hazard Control and Monitoring

GMPs GMP to control recontamination after processing
Performance criteria Processing to achieve at least 8-log reduction for salmonella
Hazard analysis, method(s) of control, and CCPs Pasteurization
Process/product criteria Time and temperature specifications for
HACCP implementation and verification Monitor environment after pasteurizer by testing for indicator organisms
and Salmonella to document effectiveness of GMPs
Microbiological criteria (if necessary) Testing product is not recommended

essary, to further verify that the process- duce and other agricultural commodities nure can contain pathogens that can
ing safety objective has been met. at the farm level. The Guide to Minimize reach fresh produce in the field or nearby
Microbial Food Safety Hazards for Fresh water supplies. Evidence indicates that
Good Agricultural Practices Fruits and Vegetables, published by FDA’s some pathogens can survive for extended
Center for Food Safety and Applied Nu- periods of time in the soil and on pro-
It is impossible to guarantee that trition (FDA/CFSAN, 1998), lists basic duce (Rangarajan et al., 2000). Manure
crops will be free of all harmful microbio- principles to guide farmers and farm should be composted to effectively elimi-
logical contamination because disease- workers on pre-harvest safety. nate pathogens and applied appropriate-
causing organisms have too many oppor- Management and control of manure ly to minimize the possibility of patho-
tunities to enter the food system through has become a critical issue in GAPs. gen survival and subsequent crop con-
the production sector. Nonetheless, it is Properly treated manure can be an effec- tamination.
possible to minimize the food safety risks tive and safe fertilizer, but untreated, im- Irrigation water also is a key factor.
and take preventive steps to protect pro- properly treated, or recontaminated ma- The source of irrigation water should be


L. monocytogenes in Ready-To-Eat Meats Escherichia coli O157:H7 in Ground Beef Patties

Listeriosis has been associated with certain Outbreaks of illness associated with undercooked ground beef
ready-to-eat (RTE) meats, including hot dogs

Listeriosis is a rare but serious disease affecting immunocompromised E. coli O157:H7 infections can result in moderate to severe disease or
individuals and the developing fetus death; children under 5 years and the elderly are the most sensitive
L. monocytogenes is a frequent contaminant E. coli O157:H7 is frequently present on the hide and in the intestines of
in certain RTE foods (e.g., up to 5%) cattle. The occurrence of E. coli O157:H7 in ground beef is estimated as
<1% in the U.S.
The majority of cases appear to be associated with dose levels in excess Fewer than 100 cells can cause disease, especially among young
of 104 CFU/serving of RTE meats (FAO/WHO, 2001) children

Estimated median number of cases per serving: 3 x 10-6 for perinatal One estimate found 26 x 104 patties per year nationwide may contain
populations; 5 x 10-8 for elderly populations; and 5.9 x 10-9 for viable E. coli O157:H7 after cooking
intermediate populations (FDA/CFSAN, USDA/FSIS, CDC, 2001)

Based on epidemiologic data. FSO set at no more than 100 CFU/g of L. To achieve a 25% reduction in the number of illnesses, the FSO may be
monocytogenes in RTE meats when consumed a concentration of E. coli O157:H7 in ground beef of no more than 1/
250g (equivalent to 1 cell per two 125g patties)

GMP to control recontamination after processing GMP to minimize contamination during slaughter and processing
Processing must result in 6-log reduction of L. monocytogenes Performance criteria cannot be specified at this time
Thermal processing Moist heat and/or acid sprays
Time and temperature for cooking Parameters for sanitation and control measures (prevention of contami-
nation during slaughter and decontamination) may be defined
Emphasis on environmental testing to verify sanitation. Consider options Sanitation and control parameters are monitored
to control pathogen growth if food should become contaminated.
Product testing is of little value in controlled environments but should be Testing of raw materials may enable plants to select suppliers with
considered when control is uncertain and pathogen growth can occur in desired microbial quality. Lot testing may be conducted to identify high
the product prevalence lots, but lots that test negative cannot be considered free of
the pathogen or “safe”

known, and periodic testing may be ap- imized wherever possible. dustry to protect food while under its
propriate. The hygiene of field workers should control—are well defined and estab-
For pathogen control, GAPs include be maintained, monitored and enforced. lished in post-harvest food processing.
recommended practices prior to planting Employees should have clean restrooms These conditions and practices provide
(Rangarajan et al., 2000). Where possi- with access to soap, clean water and sin- the basic environmental and operating
ble, the field should be upstream of the gle-use towels. All employees should be conditions that are necessary for the pro-
farm’s animal housings, and plans properly trained to follow good hygienic duction of safe, wholesome food. These
should be put in place to prevent any practices (FDA/CFSAN, 1998). conditions and practices, many of which
runoff or drift from animal operations are specified in federal, state, and local
from entering the field. Grazing livestock Good Manufacturing Practices regulations and guidelines, are now con-
should be located away from produce sidered to be prerequisite to the develop-
fields, and traffic of wild and domestic Current GMPs—the conditions nec- ment and implementation of effective
animals in produce fields should be min- essary for each segment of the food in- HACCP plans (NACMCF, 1998). GMPs

cover sanitation issues, such as equip- Some current food safety regulations could be a pH value. Process and prod-
ment design and cleaning, and pest con- (i.e., performance standards) mandate uct criteria may be used alone or in
trol. specific pathogen reductions as a result combination. Control of spores of
of processing, but this approach would Clostridium botulinum could be accom-
Performance Criteria not ensure compliance with an FSO. plished with a process criterion of heat-
For example, under the current system, ing low acid foods for a specified time
FSOs are met using performance a performance standard may require a at a specified temperature, or with a
criteria, which are the required out- 5-log reduction in pathogen levels for a product criterion of reducing the pH
come of a control step or a combina- raw agricultural commodity (e.g., fresh below a specified level for acidic foods.
tion of steps. At certain points in food juice) (see Fig. 9). Although a food pro- Often, more than one combination of
processing, control measures can be cessor could design a system to achieve criteria will meet the processing safety
applied to either prevent an unaccept- the required reduction, a higher base- objective. The specific values for a par-
able increase in a microbiological haz- line level of pathogens could result in ticular process are established as criti-
ard or reduce the hazard to an accept- higher pathogen levels after processing. cal control limits through the HACCP
able level. Chilling cooked meats and Under the FSO approach, the processor process (see below).
stews prevents the growth of Clostridi- would know the level of hazard that is
um perfringens (i.e., increase of a haz- allowed in the final product and would HACCP
ard), and pasteurization of milk or fruit calculate the performance criteria based
juices eliminates enteric pathogens (i.e., on the initial number of pathogens. HACCP is a management tool used
decrease of a hazard). The perfor- by the food industry to enhance food
mance criteria are the reduction neces- Process and Product Criteria safety by implementing preventive mea-
sary (e.g., a 5-log reduction) to achieve sures at certain steps of a process.
the processing safety objective; they are Performance criteria are imple- When HACCP principles are properly
calculated from the baseline level of the mented through application of process implemented, microbiological hazards
microbial hazard (see Fig. 8). Perfor- and/or product criteria, which are the that have the potential to cause food-
mance criteria also may address the variables in the control process or the borne illness are controlled, i.e., pre-
prevention of pathogen growth (e.g., characteristics of the product that vented, eliminated or reduced to an ac-
less than 1-log growth). achieve the necessary reduction or limit ceptable level.
Under the FSO approach, it is im- pathogen growth. A process criterion The pathway to HACCP began in
portant not to confuse performance could be the time and temperature of a 1959 because existing quality control
criteria and performance standards. thermal process; a product criterion techniques could not provide the de-
sired level of safety for food produced
for the space foods program (Bauman,
Fig. 8. Establishing Performance Criteria 1992). Traditional microbiological test-
ing of finished product was impractical
and ineffective because of the small
Baseline 106
quantities of food produced, and the
processing 5 log reduction = performance criteria
high product cost limited the amount
facility available for sampling. In addition, the
Processing food industry had no uniform approach
safety objective 101
to managing food safety. HACCP was
developed to meet this need.
Over the years, the fundamental
concepts that comprise a HACCP pro-
106 gram have been refined, and their appli-
Agricultural 1 log reduction affects facility baseline cation has become more practical. The
Baseline 105 U.S. National Advisory Committee on
Microbiological Criteria for Foods
processing 4 log reduction = performance criteria (NACMCF)—a federal advisory com-
facility mittee assembled to provide impartial,
Processing scientific advice to federal food safety
safety objective 101
agencies for use in policy develop-
ment—has revised and expanded the
original principles based on industry
experience (NACMCF, 1992; 1998). The
Baseline 101 committee consists of experts in micro-
biology, risk assessment, epidemiology,
no reduction required;
processing performance criteria = limit/prevent growth public health, food science, and other
facility and/or contamination relevant disciplines. At the same time as
Processing the NACMCF activities, Codex adopted
safety objective 101
a similar HACCP document (CAC,
1997c). NACMCF adopted seven


Fig. 9. Unequal Levels of Food Safety fruits and vegetables (see GAPs, p. 72).
For HACCP to be successful, it is
critically important that regulatory pol-
108 icy be based on the best science current-
ly available. In an effort to ensure dili-
gent HACCP implementation, regulato-
Baseline 108 106 Baseline
ry agencies may constrain the process
Food Food and ultimately undermine HACCP’s
processing 5 log reduction processing
scientific basis. Although it is an ex-
tremely useful hazard management tool,
Pathogen 103 101 Pathogen HACCP is not appropriate for all situa-
level level
tions. Regulatory policies must allow
the flexibility to apply science in a prod-
uct- and process-specific manner that
best achieves the FSO. Some current
HACCP principles: the food industry in the United States policies mandate the development of a
Principle 1: Conduct a hazard and throughout the world beginning in HACCP plan, even when a scientific
analysis. the 1990s and continuing to the present. analysis fails to identify a point in the
Principle 2: Determine the critical While many companies voluntarily process that meets the CCP criteria; it is
control points. adopted HACCP as part of their respon- impossible to have a valid HACCP plan
Principle 3: Establish critical limits. sibility to provide safe food, it also be- without a critical control point. In addi-
Principle 4: Establish monitoring came mandatory for some U.S. compa- tion, certain policies generally prescribe
procedures. nies under new regulations. In 1995, the the CCPs, without regard to the particu-
Principle 5: Establish corrective Food and Drug Administration (FDA) lar circumstances at a given food manu-
actions. published a rule that required all seafood facturing facility. As a result, the food
Principle 6: Establish verification processors and, in effect, those compa- industry may pursue mere regulatory
procedures. nies exporting to the United States to de- compliance, following the form of
Principle 7: Establish record- velop and implement HACCP systems by HACCP without its proper substance.
keeping and documen- Dec. 18, 1997. In July 1996, USDA pub- HACCP is a science-based hazard man-
tation procedures. lished a final rule that required all meat agement tool, not purely an administra-
The fundamental HACCP principles, and poultry processors to implement a tive system. When critics claim that
associated definitions, and principles of HACCP system. On Jan. 19, 2001, FDA HACCP has failed, the failure is often in
application were intended to help the food published a rule that requires large juice applying science and the HACCP prin-
industry implement food safety manage- processors to implement HACCP by ciples to managing food safety.
ment systems. First, companies identify 2002, with later compliance dates for
hazards that have the potential to cause smaller companies. These regulations Microbiological Criteria and Testing
illness or injury to the consumer and de- are playing a major role in HACCP
termine whether or not these hazards are adoption in the food industry. Routine microbiological testing can
significant. For significant hazards, the Successful HACCP implementation be useful in certain applications. It can
company identifies critical control points has not been limited to food processing. be helpful for surveillance purposes and
(CCPs) in the food system, where possi- HACCP has been used worldwide to im- process verification, and it is sometimes
ble, and establishes critical limits for their prove food safety in food service and re- helpful for lot acceptance. However, mi-
control. Critical limits are based on evi- tail, and food distribution. crobiological testing of finished product
dence that the control is effective in prac- The application of HACCP to pro- can be misleading, and negative test re-
tice. Next, CCPs must be monitored to duction agriculture, however, is limited. sults do not ensure safety. Statistical lim-
assure critical limits are not violated. This Applying the HACCP principles reveals itations of microbiological testing are of
monitoring must be a systematic proce- few, if any, CCPs in the production of significant concern, especially when the
dure that verifies that the HACCP system raw agriculture commodities. A CCP is a rate of contamination is very low. As the
is functioning as intended and that it is ef- point in the process where control can be defect rate in the product becomes low,
fective. Finally, the company must main- applied and where the control is essential emphasis should shift to improving the
tain comprehensive records associated to prevent or eliminate a food safety haz- implementation of food safety manage-
with the HACCP system. ard or to reduce it to an acceptable level ment strategies, such as HACCP, rather
HACCP is an essential part of imple- (NACMCF, 1998). The difficulty in pro- than relying on microbiological testing.
menting an FSO. Through the identifica- duction agriculture is two-fold: identify-
tion of CCPs, the process and/or product ing the source of a hazard and finding an Statistical Limitations to Testing
criteria can be translated into process- effective control. Additional research is
specific critical limits. Monitoring of needed to develop methods that effective- To analyze food for microbiological
these critical limits ensures that the per- ly control hazards in the production ag- agents, a sample of the product must be
formance criteria are met. riculture environment. Currently, haz- taken. Ideally, the sample or samples tak-
Using the principles identified in the ards in this part of the food system are en from a production lot of food will in
NACMCF and Codex documents as a most effectively controlled by GAPs, such some way reflect the whole of the lot, the
standard, HACCP was widely adopted by as those recommended by FDA for fresh underlying concept in statistically-based

Table 13. Probability of Acceptance (Pa) of Defective Product Using a 2-class utility for detecting pathogens in certain
Sampling Plan with n=10 to n=300 and c=0 (ICMSF, 2002) types of food; however, as the prevalence
rates decrease, testing becomes less reli-
Composition able for detecting contaminated lots,
of lot Number of Samples even with large numbers of samples. For
Percent many foods there is a favorable history
defective 10 20 30 50 100 200 300 of safety, and testing for pathogens is not
routinely done. Thus, as more effective
1 0.90 0.82 0.74 0.61 0.37 0.13 0.05 control measures are adopted by indus-
2 0.82
try and the prevalence of contamination
0.67 0.55 0.39 0.13 0.02 <
decreases, a point is reached where prod-
3 0.74 0.54 0.40 0.22 0.05 < uct testing is no longer practical or justi-
fiable. At that stage, greater benefit can be
4 0.66 0.44 0.29 0.13 0.02
achieved by shifting verification proce-
5 0.60 0.36 0.21 0.08 0.01 dures to comprehensive analysis of con-
trol systems that have been validated to
6 0.54 0.29 0.16 0.05 < control the pathogens of concern.
7 0.48 0.23 0.11 0.03 The effectiveness of a sampling plan is
influenced by a number of factors such as
8 0.43 0.19 0.08 0.02 whether random samples can be collected
9 0.39 0.15 0.06 0.01 from a lot of food, how samples are pre-
pared to obtain analytical units, and the
10 0.35 0.12 0.04 0.01 sensitivity and reliability of the analytical
method. Sensitive analytical methods do
not exist for many of the pathogens re-
sponsible for foodborne illness. This in-
sampling plans. So-called “lot accep- of 1%, there is a 5% probability that the cludes the viruses that have been estimat-
tance sampling plans” are in widespread defect will be not be detected and the lot ed to be responsible for more than 50% of
use around the world to determine will be accepted. all U.S. foodborne illness caused by
whether or not a food product meets a • If 10 samples are collected from known pathogens (Mead et al., 1999).
certain set of specifications. These speci- across a lot of food that has a defect rate Lot acceptance sampling plans as-
fications can target maximum numbers of 10%, there is a 35% probability that sume the microbial population is ran-
of bacteria per unit size that are set by a the defect will not be detected and the lot domly distributed throughout each lot of
purchaser of the food or by govern- will be accepted. food that is to be sampled. In reality, this
ments. When applied to determining The implications of the table be- is often not the case, particularly for
food quality, lot acceptance sampling come apparent when the prevalence of foods that are not liquids. Nonrandom
plans in conjunction with 2- or 3-class contamination for various foods is con- distribution of pathogens is a major con-
sampling plans (ICMSF, 1986; 2002) are sidered. For example, during the years tributing factor to the unreliability of
of some value. 1998-2000, the U.S. Department of Agri- product testing to prevent contaminated
The acceptance of a “quality-only de- culture (USDA) monitoring program food from entering the food supply. This
fect” that will occur occasionally no mat- for salmonella in raw meat and poultry is a particular problem for detecting E.
ter how rigid the sampling scheme is detected a range of prevalence in vari- coli O157:H7 in ground beef where the
quite different from a situation in which ous commodities (see Table 14). Con- prevalence rate is less than 1%. In this
consumer health is at risk. When sam- tamination in some foods is much more case, the current USDA Food Safety and
pling food for pathogens, sampling has likely to be detected by sampling when Inspection Service (FSIS) sampling plan
sufficient inherent limitations to be ren- the prevalence of the pathogen is high,
dered misleading. The following are as compared to foods with a lower de-
some examples of the possible conse- fect rate. However, the prevalence of Table 14. USDA Monitoring Program for
quences of rigorous sampling plans contamination for many foods is more Salmonella (1998-2000) (USDA/FSIS, 2000)
when applied to making accept/reject de- likely to be at the lower end of the scale,
Product Samples Positive
cisions for safety reasons. particularly in the case of ready-to-eat
Most microbiological sampling plans (RTE) foods. For example, the preva- Broilers 22,484 10.2%
involve anywhere from a single sample to lence rate for L. monocytogenes in RTE
as many as 60 samples per lot. Table 13 foods during 1994-1998 was reported to Market hogs 8,483 7.0%
indicates that: be from 1.08% to 4.91% (FDA/CFSAN, Cows/bulls 3,695 2.1%
• If 10 samples are collected from USDA/FSIS, CDC, 2001), and the prev-
across a lot of food that has a defect rate alence rate for L. monocytogenes in most Steers/heifers 2,088 0.3%
of 1%, there is a 90% probability that the categories of ready-to-eat meat and Ground beef 50,515 3.7%
defect will not be detected and the lot will poultry products was below 5% (Levine
be accepted. et al., 2001). Ground chicken 735 14.5%
• If 300 samples are collected from The above examples demonstrate Ground turkey 29.2%
across a lot of food that has a defect rate that microbiological testing can have


Value of Test Results
depend on the inherent sensitivity and and holds. These costs are inevitably
The usefulness of sampling as ap- specificity of the test, they also depend passed on to the consumer, in ex-
plied in certain, more recent food- upon the prevalence of contamination change for little public health benefit.
borne pathogen analysis situations has (see Fig. 10 ). The relationship between contami-
been hotly debated. For highly infec- In the case of a contaminant that nation of food, pathogen test results,
tious human pathogens, it is virtually has a high frequency of occurrence in a and public health impact is indeed a
impossible to sample sufficient vol- given food, testing may have consider- complex one. In an ideal world, per-
umes of food to assure the total ab- able value because of the higher proba- haps a better criterion of testing effica-
sence of pathogens. Moreover, there is bility that the contaminant will be cy would be based on the ability of the
real danger in assuming that if a food present in a representative sample, and, test to accurately predict disease. For
is sampled for pathogen X, and that given adequate test sensitivity and spec- this to work, a number of critical fac-
pathogen is not found, the food is safe. ificity, the predictive value of positive tors would need to be in place. First
Because sampling cannot assure safe- and negative test results will be high would be the recognition that patho-
ty, other means to do so must be (i.e., in excess of 90%). Therefore, the gen contamination may occur as non-
found or applied. test is reasonably predictive of the true random, rare events that require very
Relying on negative test results as nature of contamination. large samples to provide any confi-
an indicator of the food’s safety creates However, considering that the preva- dence of finding positives if they exist.
a disincentive to pursue additional lence of contamination by nearly all The second is the positive/negative
safety measures. Consumers with a foodborne pathogens is quite low in predictive value of the tests. Third is
false sense of security may relax their most food commodities, the combined time-to-results and cost of tests.
vigilance with regard to food safety in effect of low sampling plan efficacy and Fourth is converting true positive re-
preparation and handling. Industry low positive predictive value means that sults into a prediction of public health
and regulatory agencies may hesitate the value of testing is relatively minimal. impact. And fifth is having to deal with
to adopt new technologies that provide The chance of obtaining a sample that the public health impact of false-nega-
a superior level of food safety, mistak- has the pathogen of interest is quite tive results, which even for a test with
enly believing that the cost would not small, and nearly all presumptively posi- 95% sensitivity, will occur for 5% of
be justified because negative test re- tive tests will be confirmed as negative af- contaminated samples anyway. In es-
sults indicated present processing ter additional testing. This means a tre- sence, when we establish a zero-toler-
technologies were fully controlling the mendous expenditure for testing with ance standard, it is more based on our
hazard. very little value with respect to detecting inability to predict the no effect level
Validity is defined as the ability of contamination and potentially signifi- than it is our unwillingness to accept
the test to do what it is intended to cant costs associated with product recalls even a single illness.
do—in this case, to detect the target
microorganism if it is present, and to
not detect it if it is absent. Two com-
monly used measures of test validity Fig. 10. Predictive Value (PV) of Test Results
are sensitivity and specificity. Sensi-
tivity is the probability of a sample
testing positive if contamination is (prevalence) (sensitivity)
PV(+) =
truly present, while specificity is the (prevalence) (sensitivity) + (1-prevalence) (1-specificity)
probability of a sample testing nega-
tive if the organism is truly absent.
Both of these measures are inherent
Contaminant/food combination of relatively high prevalence
to the test itself, and fortunately, most
tests currently available for food-
Campylobacter jejuni in raw poultry: (0.60) (0.95)
borne pathogens are highly sensitive 60% prevalence; PV(+) =
and highly specific, frequently in the Test sensitivity and specificity of 95% (0.60) (0.95) + (0.40) (0.05)
range of 95% for both measures.
The predictive value of testing is an PV(+) = 0.966, or 96.6% of the time the test is positive, the sample is truly contaminated
essential concept in the attempt to un-
derstand the value of testing. Positive
predictive value is the probability that Contaminant/food combination of relatively low prevalence
the product is indeed contaminated
given that the test is positive, while the E. coli O157:H7 in raw beef: (0.01) (0.95)
negative predictive value is the proba- 1% prevalence; PV(+) =
Test sensitivity and specificity of 95% (0.01) (0.95) + (0.99) (0.05)
bility that the product is free of con-
tamination given a negative test result.
While predictive value determinations PV(+) = 0.161, or only 16.1% of the time the test is positive, the sample is truly contaminated

involves 13 analytical units weighing 25g sible that food containing either bacte- processing conditions, it should be ex-
each and a very sensitive analytical meth- ria at a prescribed level was unsafe. pected that these pathogens will be pe-
od. Aside from the low prevalence, there The “zero tolerance” for L. monocy- riodically introduced into the food
is strong evidence indicating that this togenes in RTE foods was established as processing environment by various
pathogen is not randomly distributed a safety-related criterion. The “zero pathways. To prevent the pathogens
within production lots of ground beef tolerance” actually means that L. from becoming established and multi-
from large commercial grinding opera- monocytogenes must be absent from plying, the sampling program should
tions. two 25g samples of foods under FDA aggressively look for these pathogens.
The criteria for most infectious inspection. The total absence require- Finding a positive sample should be
agents involve 2-class sampling plans ment was derived at a time when there treated as a success, because corrective
and presence/absence testing. The strin- were no effective methods for finding actions can then be applied and con-
gency of the sampling plan is deter- L. monocytogenes in food (or any envi- sumer protection assured. Treating a
mined by the number of samples ana- ronment outside of the human or ani- positive sample as a failure and apply-
lyzed and the number of allowable posi- mal). There was no understanding of ing a penalty decreases the desire to de-
tive samples. Sampling plans that do not the very widespread existence of L. tect the pathogens, discouraging the
allow any positive sample units have monocytogenes throughout the envi- aggressive nature of the environmental
been used for a variety of pathogens ronment, including food processing sampling program.
(e.g., salmonella and L. monocytogenes environments, nor an appreciation of
in RTE foods, and E. coli O157:H7 in the number of foods in which the bac- Testing Methods
raw ground beef). Some have referred to teria historically had been present.
sampling plans that do not allow any Thus, contemporary knowledge about Disease surveillance and control ef-
positives as “zero tolerance.” In reality, human exposure suggests that many forts will benefit greatly from new
the zero tolerance can be made more or humans are routinely exposed to the pathogen detection methods that offer
less stringent by increasing or decreas- bacteria with no consequence to health, greater precision, rapid results, and de-
ing the number of samples. Thus, a although L. monocytogenes does cause creased cost. However, efforts to adapt
sampling plan could specify 5, 10, 20 or illness in sensitive subpopulations. these new technologies to the challeng-
more samples. Although 25g analytical The “zero tolerance” has acted as a dis- es in the food environment are ongo-
units are normally used, sampling plan incentive for the application of quanti- ing.
stringency also could be increased by tative (enumerative) methods, and Many methods of detection are cur-
increasing the size of the sample unit, thus, the body of human exposure data rently available for foodborne patho-
for example, to 50g. is incomplete. gens, but food microbiologists must of-
Today, there is growing acceptance ten choose between enumeration and
Microbiological Criteria of the need for management systems identification without the option of
based on GMPs and HACCP to control both. Enumerative methods are usually
Historically, attempts have been food safety hazards. Microbiological based on the ability of the normal
made to apply microbiological criteria testing is sometimes valuable in verify- healthy bacterial cells to multiply in a
for the purpose of classifying foods as ing the effectiveness of GMP and nutrient-rich medium. Although selec-
either microbiologically acceptable, or HACCP systems and validating CCPs tive agents are sometimes added to favor
microbiologically unacceptable. In within HACCP systems. There may be the growth of a specific group of organ-
1985, the Food and Nutrition Board of a role for testing certain ingredients isms, most of these methods are still
the National Research Council (FNB/ when they can influence the safety of a reasonably nonspecific. With respect to
NRC) addressed the subject of micro- finished product, but because the test- pathogen identification, methods have
biological criteria, and found that such ing of ingredients faces the same weak- historically relied on cultural enrich-
criteria were of limited use, particular- ness as end-product testing, auditing ment to increase the numbers of the tar-
ly if safety assurance is the goal, and of suppliers’ control programs has in- get microorganism and allow resuscita-
that HACCP should be applied wher- creased to provide greater assurance. tion of injured cells. When followed by
ever possible for safety assurance In addition to product testing, en- selective and differential plating, these
(FNB/NRC, 1985). The HACCP sys- vironmental testing may be necessary. methods provide discrimination of the
tems envisioned by the FNB/NRC did Salmonella and L. monocytogenes have target organism from the background
not rely on end-product testing for the ability to become established as microflora, but are non-enumerative.
pathogens, but rather, if analyzed mi- residents in food processing establish- For both enumerative and non-enu-
crobiologically at all, analyses were ments. Environmental sampling pro- merative methods, the combined effect
performed at points along the food’s grams assess the degree of control and of low levels of contamination and the
production chain, particularly to verify indicate when corrective actions are need for cultural growth results in
that CCPs were under control. needed. They may or may not indicate lengthy assays, frequently extending be-
Microbiological criteria considered a safety problem in the finished prod- yond four days for even preliminary re-
by FDA generally include standard uct. sults.
plate count, coliform counts, yeast and The optimal regulatory approach to Most rapid method developments
mold counts, and E. coli (generic) environmental testing would use our have sought to shorten detection time
counts. Coliforms and E. coli were be- understanding of basic human nature by replacing the selective and differen-
lieved to be indicators of possible fecal to encourage and reward diligence. De- tial plating steps with more rapid tech-
contamination, and therefore, it is pos- pending on the type of food and the nologies such as ELISA and DNA hy-


emerging molecular detection methods,
including biosensors (deBoer and
Testing for Mycotoxins Beumer, 1999) and microarray technol-
In the United States, raw agricul- diverted early in the food processing ogy (Epstein and Butow, 2000), must be
tural commodities are routinely chain. A similar approach is linked tempered with an appreciation for the
screened for mycotoxins using specific with an indemnification program for complexity of the food matrix.
FDA guidelines that are based on hu- peanuts, which are also highly suscep-
man risk assessments. The testing tible to aflatoxin contamination. Surveillance for Foodborne
methods used must be validated by Analogous guidelines have been set Hazards and Illness
the AOAC International (Gaithers- for other mycotoxins (trichothecene
burg, Md.), which ensures reliability deoxynivalenol and the fumonisins), One way to identify emerging patho-
and reproducibility. and rapid tests are available. gens is surveillance of foodborne illness.
Some methods, such as commer- In general, careful monitoring of Not only can scientists track the spread
cial enzyme-linked immunosorbent weather conditions and field testing and frequency of a pathogen by looking
assays (ELISAs), are particularly use- for mycotoxins will identify years in for its victims, they can quickly spot
ful for rapid screening of commodities which there is increased potential for changes in virulence or exposure. Sur-
and take as little as 5 minutes to com- contamination in specific commodi- veillance data can be used for quick out-
plete (Pestka et al., 1995). Because ties. Screening efforts can be in- break response and also as the basis for
corn is susceptible to aspergilli that creased and targeted toward possible qualitative and quantitative risk assess-
produce aflatoxins, it is screened at the problematic materials and regions, ment. New scientific tools have signifi-
grain elevator and rejected if it exceeds such as aflatoxins in corn and peanuts cantly increased the speed and depth of
the FDA guideline. Thus, aflatoxin- during an extended drought in the surveillance information gathering, mak-
contaminated corn is identified and southeastern United States. ing it more effective.

Purposes and Mechanisms

bridization, but because these methods that inhibit PCR enzymatic reactions; Surveillance involves the systematic
remain hampered by less than optimal (3) detect low levels of contaminating collection of data with analysis and dis-
assay detection limits, lengthy cultural pathogens; (4) assure detection of via- semination of results. Surveillance sys-
enrichment steps are still necessary. ble (infectious) pathogens; and (5) con- tems may be passive or active, national
Furthermore, cultural confirmation for firm molecular amplification products or regional in scope, or based on a senti-
presumptively positive results is gener- with more lengthy DNA hybridization nel system of individual sites. Tradition-
ally required for regulatory purposes. assays (Bej and Mahbubani, 1994). ally, human foodborne disease surveil-
The limiting factor in making these With respect to the first three chal- lance has been conducted for three rea-
methods truly rapid is predominantly lenges, the application of rapid methods sons: (1) to identify, control, and prevent
the lengthy incubation time required to could perhaps be improved if pathogens outbreaks of foodborne disease, (2) to
increase cell numbers. were separated, concentrated, and puri- determine the causes of foodborne dis-
Enzymatic nucleic acid amplifica- fied from the food matrix before detec- ease, and (3) to monitor trends in occur-
tion methods such as the polymerase tion (Swaminathan and Feng, 1994). rence of foodborne disease.
chain reaction (PCR) offer several po- None of the various bacterial concen- By identifying outbreaks and their
tential advantages for the rapid and reli- tration methods, including the most causes quickly, surveillance can result in
able detection of microbial pathogens in widely used immunomagnetic separa- early intervention to address hazards in
foods. The primary advantage of this tion, (Sharpe, 1997) is ideal, highlight- the food supply. Officials may be able to
technology is the theoretical replace- ing the need to increase research in this remove contaminated products from re-
ment of cultural enrichment with spe- area. With respect to detection of viable tail shelves (e.g., identification of Sal-
cific nucleic acid sequence enrichment, pathogens, naked DNA and the DNA of monella Agona in contaminated cereal
thereby decreasing total detection time. dead cells can persist for long periods of (CDC, 1998c)) or rectify inappropriate
There are many reports of PCR-based time (Herman, 1997). Even the more food handling procedures (e.g., under-
assays for the detection of foodborne stable 16S rRNA is not an ideal indica- cooking of meats or cross-contamina-
pathogens and several companies mar- tor of pathogen viability (McKillip et al., tion of vegetables from raw chicken).
ket these systems, all of which are cur- 1998). Although mRNA may be consid- The cumulative information ob-
rently in evaluation for AOAC approval. ered a more promising target (Sheridan tained through surveillance and out-
In reality, rapid molecular detection et al., 1998), key assay design issues break investigation can reveal the magni-
methods for pathogens in food prod- would need to be addressed. Finally, tude and trends of foodborne disease,
ucts remain in the developmental stages. methods to simplify or even eliminate helping policy makers identify optimal
The significant methodological hurdles post-amplification confirmation assays prevention strategies (Borgdorff and
yet to be addressed include the need to: (McKillip and Drake, 2000; Norton and Motarjemi, 1997). Additionally, im-
(1) test larger, realistic sample volumes Batt, 1999; Sharma and Carlson, 2000) proved understanding of disease and
(at least 25 ml or g) instead of the small are expensive and have not been widely hazard etiology can help researchers an-
volumes (10-50 microliters) used in applied to food matrices (Koo and ticipate or recognize new problems, such
molecular-based assays; (2) account for Jaykus, 2000). as toxins in one food that could pose a
the effect of residual food components When taken together, the promise of problem in other foods or toxins that are

Outbreak Investiga-
and reports of illnesses among food han- with enteropathogenic (EPEC) and
tions and New dlers led to early concern that the restau- enterohemorrhagic (EHEC) E. coli and
rant was experiencing a large outbreak of EAST1 (astA), a heat-stable enterotox-
Foodborne Pathogens viral gastroenteritis. However, as the in associated with enteroaggregative
On April 29, 1991, local public clinical and epidemiologic features of the adherent (EaggEC) E. coli. Thus, the
health officials were notified of an out- outbreak emerged from interviews with outbreak strain did not fit neatly into
break of foodborne illness among per- patrons, it appeared typical of previously any of the recognized categories of di-
sons who celebrated “Secretary’s Day” described outbreaks caused by entero- arrheagenic E. coli and would not have
at a local restaurant (Hedberg et al., toxigenic E. coli (ETEC). been identified as a pathogen had it
1997). Seventeen (89%) of 19 mem- The recognition that the outbreak not been implicated in this outbreak.
bers of the index group developed di- may have been caused by an uncommon The majority of diarrheagenic E.
arrhea and cramps 11 to 122 hours foodborne pathogen led to extensive ef- coli virulence factors are encoded on
(median, 56 hours) after their meal. forts to obtain stool from ill patrons to pathogenicity islands, transmissible
Fewer than half of cases reported nau- confirm the etiology. A lactose-negative plasmids, bacteriophage, or trans-
sea, myalgia, fever, or vomiting. Dura- non-motile E. coli O39 was isolated from posons. Horizontal transmission of
tion of illness ranged from 4 to 7 days 10 of 22 cases. No Salmonella, Shigella, virulence factors led to the development
(median, 5 days). Similar illnesses Campylobacter, Yersinia, Vibrio, or Plesi- of highly virulent E. coli O157:H7
were also reported among other res- omonas species were isolated from ill pa- which has emerged as a major food-
taurant patrons and among five (15%) trons. Although the clinical and epide- borne disease of public health impor-
of 34 food handlers at the restaurant. miologic features of the outbreak sug- tance. This same genetic plasticity
The restaurant served a large hotel gested ETEC, the outbreak-associated could lead to emergence of other com-
and conference center and featured an O39 strain did not possess ETEC heat- binations of virulence factors. Prompt
elaborate buffet with a variety of fresh labile (LT) or heat-stable (ST) enterotox- and thorough epidemiologic investiga-
fruits, vegetables, salads, and gourmet ins. Extensive testing of the outbreak-as- tion of outbreaks will be needed to
food items that combined cooked and sociated strain by a battery of gene identify these novel emerging patho-
uncooked foods. The apparent high probes detected the presence of intimin gens and to further our understanding
attack rate of illness in the index group (eae), an adherence factor associated of their public health significance.

newly recognized as a human health haz- clined 48% during 1996 -1999, suggest- by an uncommon Salmonella serotype.
ard (see sidebar above). ing that these control strategies are be- Epidemiological investigation of these
HACCP systems rely on accurate ginning to work (CDC, 2000a, b). cases identified the source.
knowledge of potential hazards (NACM- PHLIS has developed an automated
CF, 1998). Many of these hazards—spe- Current Surveillance Programs surveillance outbreak detection algo-
cific agents, food ingredients, or agent/ rithm (SODA), originally developed to
food interactions—were originally iden- Foodborne disease surveillance address Salmonella, that uses the 5-year
tified as a result of foodborne disease consists of four primary components: mean number of cases from the same
surveillance. Because food sources and (1) identifying and reporting outbreaks, geographic area and week of the year to
foodborne disease agents are constantly (2) monitoring for specific pathogens, look for unusual case clusters (Hutwag-
changing, hazard analysis is an ongoing (3) determining risk-factors for sporadic ner et al., 1997). S. Stanley and S. Agona
process that requires continuous support cases of infection with common food- infections initially identified by individu-
from public health surveillance of food- borne pathogens, and (4) studying the al state health departments were discov-
borne disease. population to track gastrointestinal ill- ered to be multi-state outbreaks based
Foodborne disease surveillance can ness, including trends in the requests for on disease clusters identified by SODA.
also supply important feedback on the health care, food consumption and per- Because it compares current cases to
effectiveness of control strategies. For sonal prevention measures. 5-year means, SODA appears to be more
example, during the 1980s, the in- Improving pathogen-specific surveil- effective at detecting case clusters of un-
creased occurrence of sporadic S. Enter- lance has been a major focus of the Na- common serotypes rather than common
itidis infections and outbreaks in New tional Food Safety Initiative. Serotype- serotypes, such as S. Typhimurium. Al-
England led to the identification of a specific surveillance of Salmonella con- though the Minnesota Department of
new problem with S. Enteritidis con- ducted by state health departments and Health reported 11 confirmed outbreaks
tamination of grade A shell eggs (St. CDC’s Public Health Laboratory Infor- of S. Typhimurium infection from 1996-
Louis et al., 1988). In the United States, mation System (PHLIS) has identified 1998, SODA detected only three. During
USDA and FDA have worked with the several large, multi-state outbreaks of the same time period, SODA identified
egg industry to develop and implement salmonellosis. These outbreaks, caused nine weeks where the number of S. Typh-
a number of control strategies (Hogue by cantaloupes, tomatoes, and alfalfa imurium reports exceeded the 5-year av-
et al., 1997). The incidence of S. Enter- sprouts, were spotted because of unusu- erage. Six of these notifications were due
itidis infections in FoodNet sites de- al, time-related clusters of cases caused to epidemiologically unrelated S. Typh-


imurium isolates with different pulsed- uses active surveillance, meaning public States, 82% are attributed to “unknown
field gel electrophoresis (PFGE) patterns. health authorities regularly contact clini- agents” (Mead et al., 1999). Of the 28
One flagged the occurrence of two si- cians and laboratories to obtain case re- known foodborne pathogens included in
multaneous outbreaks and the other two ports. this estimate, routine passive surveillance
were due to a single outbreak that ex- Most foodborne disease surveillance systems exist for only 17 (61%). For
tended over time (Bender et al., 2001). uses passive reporting systems, in which many of the others, scientists must infer
Molecular subtyping schemes, such reports are voluntarily submitted by their frequency from the occurrence of
as PFGE, can improve the investigation health clinics and laboratories. This sys- outbreaks or from a limited number of
of outbreaks by distinguishing unrelat- tem depends on the clinician’s ability to population-based studies that researched
ed sporadic cases from the main out- diagnose the illness and the willingness the causes of diarrhea. For example, clini-
break-associated strain. The ability to of clinicians and laboratory personnel to cal laboratories do not routinely identify
distinguish specific subtypes among rel- report the diagnoses to the appropriate Norwalk-like viruses (NLVs), and no sur-
atively common organisms, such as E. public health authorities. veillance program tracks cases of NLV in-
coli O157:H7 and S. Typhimurium, is In general, active surveillance yields fection. Yet estimates attribute 11% of all
the basis of the National Molecular better data than passive systems but is episodes of diarrheal illnesses to NLVs,
Subtyping Network (PulseNet), which more expensive and limited in scope. Be- based on a study from the Netherlands
takes advantage of recent advances in cause some cases of foodborne illness (Mead et al., 1999). The estimated propor-
both molecular biology and informa- will remain unrecognized and go unre- tion of foodborne illness that is caused by
tion technology. Highly reproducible ported, even active surveillance systems unidentified agents is bolstered by Centers
PFGE patterns are generated for a are inherently incomplete (Potter and for Disease Control and Prevention
pathogen implicated in an illness, and Tauxe, 1997). (CDC) data (Mead et al., 1999). No agent
the PFGE patterns can be electronically One of the most striking gaps in our was identified in 1,873 (68%) of 2,751
shared between participating laborato- foodborne disease surveillance is gener- confirmed foodborne outbreaks reported
ries. An outbreak of E. coli O157:H7 in- ation of data about individuals who to CDC from 1993-1997 (Olsen et al.,
fections in Colorado was associated have gastrointestinal illness but do not 2000).
with consumption of a nationally dis- see a physician. Furthermore, physicians A high percentage of the outbreaks
tributed ground beef product. Within often treat mild to moderate gas- attributed to “unknown etiology” are
days, public health officials could com- trointestinal illness symptomatically probably outbreaks of viral gastroenteri-
pare the outbreak strain to PFGE pat- and do not frequently culture speci- tis that were not confirmed either be-
terns of E. coli O157:H7 isolates mens or conduct the wide range of di- cause stool samples were not available
throughout the United States (CDC, agnostic tests necessary to identify all for testing, or because public health lab-
1997). PulseNet has the potential to be foodborne agents. oratories did not perform the test neces-
the “backbone” of a public health sur- sary to detect viruses. For example, one
veillance system that can provide truly Unknown Agents retrospective study confirmed the pres-
national surveillance for a variety of ence of NLVs in 90% of a select group of
foodborne pathogens in a manner time- Surveillance for foodborne diseases outbreaks of non-bacterial gastroenteri-
ly enough to be an early warning system is based on detection of specific patho- tis (Fankhauser et al., 1998). In Minne-
for outbreaks of foodborne disease gens or the occurrence of illnesses, such sota, officials used the clinical and epide-
(Hedberg et al., 2001). as diarrhea, in defined groups. An out- miologic appearance of the outbreak to
PulseNet’s usefulness is currently break may be recognized because a state link 120 (41%) of 295 confirmed food-
limited because not all public health lab- public health laboratory detected the in- borne outbreaks reported from 1981-
oratories are connected, not all clinical creased occurrence of a specific subtype 1998 to NLVs, leaving only 26 outbreaks
laboratories routinely submit isolates to of E. coli O157:H7, or because half of the (9%) attributed to unknown agents (De-
public health laboratories, and many people who attended a specific event de- neen et al., 2000). The factors used in the
states do not have sufficient epidemio- veloped vomiting and diarrhea shortly classification included a median incuba-
logic resources to investigate individual after the event. In the first case, surveil- tion period of between 24-48 hours, a
cases or clusters. lance is limited by what clinical laborato- 12-60 hour duration of symptoms, and a
In contrast to PulseNet’s widespread ries routinely identify when processing relatively high proportion of cases expe-
surveillance area, FoodNet is a sentinel- human stool samples, whether by direct riencing vomiting (Hedberg and Oster-
site, active surveillance project designed to examination, culture, or use of non-cul- holm, 1993; Kaplan et al., 1982). In a ret-
track all diagnosed infections of impor- ture diagnostic tests. In the second case, rospective review of foodborne out-
tant foodborne diseases and evaluate the surveillance has a better chance of identi- breaks reported to CDC from 1982 to
laboratory, physician and patient practices fying foodborne agents that are not part 1989, almost half (48%) of the 712 out-
that cause an individual case to be diag- of routine clinical microbiology, but it is breaks reported as having an undeter-
nosed. FoodNet’s initial surveillance area still limited by the epidemiologic and mined etiology met the epidemiologic
(13.2 million residents of Minnesota, Or- laboratory resources available to public criteria for outbreaks of NLV (Hall et al.,
egon, and selected counties in California, health departments. 2001). Thus, although a high percentage
Connecticut, and Georgia) was expanded Published estimates of foodborne dis- of reported foodborne illnesses do not
in 2000 and 2001, adding sites in New ease occurrence highlight the limitations have an identified cause, it appears that
York, Maryland, Tennessee, and Colorado of our current surveillance system. Of the many are potentially identifiable causes.
that brought the population under sur- 76 million cases of foodborne illness esti- Additional surveillance would help re-
veillance to 33.1 million persons. FoodNet mated to occur each year in the United searchers more frequently identify the

agent responsible for cases of foodborne
illness and provide more reliable esti-
mates of the true prevalence of various Animal Surveillance for
foodborne pathogens. coli O157:H7. Of 563 ground beef
E. coli O157:H7 samples, 78.6% were contaminated
Risk assessments for specific by nonpathogenic E. coli but none by
Integrated Surveillance E. coli O157:H7 (USDA/FSIS, 1996).
pathogens such as E. coli O157:H7 in
The modern concept of public health ground beef require measurements of More recently, with the aid of
surveillance, first articulated by Alex- many parameters at every step from much more sensitive detection meth-
ander Langmuir, views surveillance as a farm to table. Surveillance programs ods, researchers found EHEC O157
process (Foege, 1996). As it relates to gather these data and reveal useful in- (E. coli O157:H7 or O157:nonmo-
food safety, the process is concerned not formation about hazards. For exam- tile) in the feces of 27.8% of cattle at
only with outcomes in the human popu- ple, E. coli O157:H7 is widely distrib- a slaughter plant; 10.7% of hides
lation but also with the occurrence of uted throughout beef and dairy cattle were contaminated, and 43.4% of
foodborne hazards in all types of foods, herds in the United States (Hancock et carcasses were contaminated before
their sources, and the various stages in al., 1998). NAHMS addresses emerg- evisceration (Elder et al., 2000). Only
their conversion to consumable food. ing issues such as the association be- 17.8% of carcasses were contaminat-
Operationally, surveillance involves the tween calf management practices and ed post-evisceration, and 1.8% of
systematic monitoring of disease and the presence of E. coli O157:H7 in cat- carcass tissues contained EHEC
hazard reports—in animal and plant tle herds (Garber et al., 1995; Losinger O157 after processing, which dem-
populations, food production and pro- et al., 1995). The veterinary Diagnos- onstrates the effectiveness of plant
cessing environments, foods and ingredi- tic Laboratory Reporting System com- sanitation processes.
ents, and in human populations— piles and analyzes reports from state Despite this relative efficacy,
through the systematic collection, analy- veterinary diagnostic laboratories to USDA detected E. coli O157:H7 in
sis, and interpretation of outcome-spe- assess trends in infectious diseases ground beef samples at a rate of ap-
cific data, closely integrated with the among food animals (Salman et al., proximately 8.7 per 1,000 samples in
timely dissemination of these data to 1988). 2001, and E. coli O157:H7 contami-
those responsible for preventing and To prepare for HACCP introduc- nation of ground beef resulted in 25
controlling disease or injury (Thacker tion in the meat industry, USDA con- recalls during 2001 (USDA/FSIS,
and Berkelman, 1988). ducted a series of baseline surveys of 2002). Regulatory agencies and food
Foodborne disease surveillance has beef slaughter plants and the ground processors need to work together to
traditionally been viewed as a subset of beef final product. At that time, only 4 advance the scientific understanding
public health surveillance. The links be- (0.2%) of 2,081 steer and heifer car- of the persistence and transmission
tween surveillance for foodborne diseas- casses and none of 2,112 cow and bull of these agents in food production
es in humans and surveillance for food- carcasses were contaminated with E. environments.
borne hazards in foods have only recent-
ly received increased attention. Food-
borne hazard surveillance monitors the
conditions that can lead to foodborne ill-
nesses (Guzewich et al., 1997). For exam-
ple, hazard surveillance systems can de- rowly focused studies of a single species in the food and water that food animals
tect microbial pathogens at various facil- in a particular segment of the produc- consume also may be appropriate
ities that handle food (e.g., farms, meat tion process. (Tauxe, 1997). If farms show evidence of
and poultry processors, and restau- Integrating the information from an increasing pathogen prevalence, then
rants). Hazard surveillance typically in- on-farm monitoring program such as prompt intervention might prevent the
volves the collection of data on food- NAHMS with processing data, retail food pathogens from eventually being con-
borne hazards in food products and surveillance, residue and antimicrobial sumed by humans.
food sources, follow-up data when haz- resistance monitoring, and subsequently Effective surveillance for food safety
ards are present at unusual levels, and with FoodNet information will be critical requires the coherent assembly of infor-
information that helps define the sources for the implementation of a true farm- mation from different sources. Integrat-
of hazards in foods. to-table approach to food safety surveil- ing animal and environmental surveil-
Animal health surveillance as it re- lance. Not only will the data be more re- lance systems into established human
lates to food safety is a component of liable if a cohesive surveillance system surveillance systems will greatly increase
foodborne hazard surveillance. Compre- monitors food from the farm to the table, our understanding of the epidemiology
hensive animal health surveillance sys- but such a system will likely provide the and sources of foodborne disease. In
tems were nonexistent until the National impetus for a more comprehensive sur- particular, an independent molecular
Animal Health Monitoring System veillance system in domestic animals subtyping system linked to PulseNet has
(NAHMS) was implemented in 1983 (Bush et al., 1990). great potential value for evaluating the
(King, 1990). Current resources limit The awareness of the need to moni- potential public health significance of
these surveillance programs; the NAHMS tor pathogens in healthy food animals is pathogens isolated all along the food
on-farm monitoring system does nar- fairly recent, and monitoring pathogens processing continuum. For example, it


would be extremely useful for a food new ways to control microorganisms method is appropriate for all circum-
processor to be able to evaluate whether that have not yet been conceptualized. stances, so selection of the best method is
a particular environmental strain of List- Another exciting area with genomics important. This technology is changing
eria isolated from a processing environ- as the driving force relates to under- rapidly, and the following information
ment had ever been associated with hu- standing the bacterium’s global gene ex- provides a brief overview of the progress
man infections. The technology exists to pression while varying the bacterium’s in this area and the future potential.
create such a system. Data privacy and environment. This has been made possi- Until recently, efforts to determine
regulatory penalties will need to be mod- ble by the development of oligonucle- bacterial relatedness relied on techniques
ified to encourage the food industry’s otide “chips” or cDNA microarrays that that assessed one or more phenotypic
full participation. enable “expression profiling,” that is, the markers. These methods include sero-
study of the messenger RNAs, and when typing, phage typing, biotyping, antibiot-
and which ones are produced. Microar- ic susceptibility testing and bacteriocin
Future Methods: the Promise of Genomics typing. Now, molecular typing methods
rays may help unravel the function of the
Since the advent of recombinant numerous genes whose functions are not can identify different clones (genetically
DNA technology, a better understanding yet known. An excellent overview of identical organisms descended from a
of how and why pathogens do what they these technologies was recently presented single common ancestor) at the bacterial
do has emerged. Progress has been by Schwartz (2000). species level. These molecular tech-
steady. In many cases, one gene at a time Using DNA microarrays, also known niques are used to physically characterize
has given up its secrets, and, in the pro- as biochips, research scientists can analyze bacteria based on their DNA composi-
cess of doing so, has presented new puz- the transcription profiles of the whole ge- tion (genotyping) or on production of
zles to be solved. The science of genom- nome for practically any microorganism proteins, fatty acids, carbohydrates, or
ics is simply the study of the genes of an of interest. For example, in organisms other biochemical content (phenotyping
organism and their function. It is now such as Haemophilus influenzae and or chemotyping).
possible to sequence entire genomes, and Streptococcus pneumoniae scientists have As technology has evolved, many
this has been accomplished for some sig- used DNA biochips to map more than previously complex processes have been
nificant human pathogens. The process 100 genes and their expression profiles. automated, miniaturized and linked to
of whole genome sequencing has been The current detection range has been be- computer control centers that guide the
accelerated by automation and the appli- tween one and five transcripts per cell, as operation, including data analysis. As
cation of sophisticated computer tech- confirmed by conventional methods such the technologies have become wide-
nologies (informatics). as Northern blot analysis. Scientists can spread, researchers are now able to gen-
Data gathered to date on pathogenic learn what gene(s) are turned on or off erate more timely data at a lower unit
bacteria have already provided revealing under different conditions by putting cost. Of particular interest to those in-
insights. For example, nearly one-half of (spotting) DNAs representing all ORFs in volved in the biochemical analysis of mi-
the open reading frames (ORFs) se- a bacterial genome and using differential- croorganisms are procedures that have
quenced have no known function. It is ly labelled cDNAs from both wild-type been adapted or are amenable to whole
clear that we have just begun to under- and mutant bacteria. cell techniques, as they offer all of the
stand how these bacteria survive and react Microarray technology affords un- conveniences of rapid and economical
to their environment. From comparisons precedented opportunities and ap- analysis. Huge libraries of customizable
among the complete sequences of bacte- proaches to diagnostic and detection computer databases are now available to
ria, it is also clear that far more horizontal methods. For example, microarrays can assist in pattern recognition for detection
transmission of genetic material has oc- be used to develop rapid identification and identification of microorganisms
curred than previously thought. Hori- systems for both pathogenic and spoilage based on analysis of whole cells, as well
zontal transmission of genes can rapidly bacteria, to conduct mutation analyses, as individual genetic elements or chemi-
transform a commensal bacterium into a and to investigate protein-DNA interac- cal derivatives. The need for quick test
potential pathogen through the sharing of tion. RNA of a related species can be results have driven these advancements.
large numbers of virulence-related genes studied using differential gene expres- Automated methods are now available
(pathogenicity islands) or genes encoding sion under less stringent hybridization for detection, identification, typing and
for antibiotic resistance. conditions (referred to as virtual expres- analysis of biological components or
Comparisons also enable the genera- sion arrays). In addition, microarrays structural changes that occur due to en-
tion of hypotheses regarding a bacteri- will be used in the future to detect organ- vironmental pressures or extraneous in-
um’s virulence potential that can then be isms or foods modified using recombi- fluences. Bench top versions of sophisti-
tested by other traditional laboratory ap- nant DNA biotechnology. For example, cated devices allow for more portability
proaches, or by further genetic manipu- transcript mapping (imaging) of wild- and efficient use of laboratory space.
lation. Comparative genomics also may type versus genetically modified organ-
lead to new approaches to phylogenetic isms can monitor changes in risk-related Genotyping Methods
classification. An adjunct to genomics is factors such as virulence genes.
proteomics, the study of the complete Genotyping has many advantages
protein complement of an organism. Al- Pathogen identification over traditional typing procedures (Olive
though it might appear that these tech- and Bean, 1999; Spratt, 1999; Tompkins,
nologies have opened up a new level of New pathogen identification technol- 1992; Versalovic et al., 1993). The major
complexity, it is believed by many scien- ogies are faster, cheaper, more powerful advantage lies in its ability to distinguish
tists that this very complexity may yield and increasingly automated. No single between two closely related strains. Oth-

er advantages of genotyping include: Salmonella (Bender et al., 2001; Van Future Issues
(1) DNA can always be extracted from Beneden et al., 1999), L. monocytogenes
bacteria so all strains are theoretically (Graves and Swaminathan, 2001; Ojenivi Although genome-based typing
typeable; (2) analytical strategies for the et al., 2000; Proctor et al., 1995), E. coli methods are increasingly powerful tools
genotypic methods are similar and can O157:H7 (Barrett et al., 1994) and virus- in molecular epidemiology, several issues
be applied to DNA from any source; (3) es (CDC, 2001), and is the method that need to be addressed if these methods are
genotyping procedures do not generally is currently being used by CDC as the to be incorporated more routinely. First-
require species-specific reagents and (4) basis for its PulseNet system. ly, one should not forget about the ad-
the methods are amenable to automa- There is a trend to use new diagnos- vantages of classifying organisms to the
tion and statistical data analysis (Arbeit, tic assays to disclose the presence of genus and species level, as well as doing
1995; Bingen et al,. 1994). Combina- pathogenic bacteria in foods or human serotyping and phage-typing for some
tions of different genotypic methods patients without isolation of the organ- bacteria, before interpreting banding
can be used to increase the discrimina- ism. This presents a challenge to micro- patterns resulting from molecular typ-
tory power of typing and fingerprinting biologists, in that many of the typing/ ing. A good example of this is a 2001 sal-
analyses. Furthermore, selection of the fingerprinting methods currently in use monellosis outbreak associated with raw
appropriate typing method can allow rely on large quantities of DNA isolated almonds that was detected only because
analysis of groups of bacteria at the ap- after amplification of the strain of inter- both serotyping and phage-typing of sal-
propriate level and rate of change. To il- est. Methodologies based on DNA se- monella isolates were done. As well, in
lustrate, ribotyping of Vibrio cholerae quencing after PCR amplification direct- the absence of a “gold standard” by
isolates responsible for the 1994 - 1995 ly from the source material may present which to judge a typing method (van
cholera epidemic in Ukraine indicated at least a partial solution to the problems Embden et al., 1993), careful standard-
that only a single strain arising from in- created by the absence of an isolate. The ization of and adherence to laboratory
troduction into that country was re- CDC PulseNet group has, for instance, protocols is essential, if individual meth-
sponsible (Clark et al., 1998). Other recently provided funding to interested ods are to be accepted for classification
more discriminatory methods were state laboratories for research into the of strains. The lack of reproducibility of
used to track the course of the epidemic. appropriate genes to be sequenced to al- certain techniques is another contentious
A combination of typing or fingerprint- low differentiation of bacterial patho- issue. Consistent reproducibility is es-
ing methods may therefore be necessary gens of interest. sential, if these methods are to be of val-
to fully characterize bacterial popula- ue in the long-term analysis and catego-
tions important to public health. rizing of bacterial strains. Another ex-
Biochemical and Chemical Methods tremely important issue is in the inter-
The most common genotypic meth-
ods currently used include: Numerous biochemical techniques pretation of minor (ca. 1 to 3) banding
• chromosomal DNA restriction anal- offer an alternative to direct nucleic acid differences between strains. Some scien-
ysis, fingerprinting. Chemotaxonomy in- tists argue that a single difference in the
• plasmid typing, volves the application of chemical and production of an enzyme or the shift of a
• DNA probe-based hybridizations physical manipulations to the analysis of single band on a gel is not enough to say
(such as ribotyping) the chemical composition of whole bac- that two isolates are different, and that
• amplified fragment length polymor- terial cells or their cellular components clonality should be considered as a rela-
phism (AFLP) to arrive at some identification or taxo- tive concept (Arbeit, 1995). In addition,
• PFGE nomic positioning. Even with accelerat- strain relatedness should only be judged
• PCR-based methods (such as ran- ed advances in technology that have al- in the presence of other data, especially
domly-amplified polymorphic DNA lowed for miniaturization and automa- epidemiologic data.
(RAPD), repetitive sequence-based PCR tion of analytical equipment, the bacteri- The ultimate goal is an “ideal” molec-
(rep-PCR), PCR-ribotyping and PCR-re- al growth period and chemical deriva- ular typing method; one that is easy to
striction fragment length polymorphism tions prior to analysis still remain the ul- perform, cost-effective, relatively rapid,
(PCR-RFLP)), and timate limiting factor with respect to amenable to statistical analysis and auto-
• sequence-based methods, including rapid analysis. Thus, methods that are mation, able to type all possible strains,
multilocus sequence typing, flagellar lo- amenable or adaptable to whole cell reproducible, and properly balanced be-
cus and flagellar short variable region se- techniques and require only minute tween increased discriminatory power
quencing (e.g., for Campylobacter), and quantities of sample and/or in situ and applicability. Rapid advances in typ-
analysis of DNA sequences of a number chemical derivations are of particular in- ing methods based on whole organism
of other genes. terest, including: DNA sequencing are helping us to ap-
PFGE has now been applied to a • mass spectrometry (MS), especially proach such an ideal method. In the fu-
wide range of microorganisms and has matrix-assisted laser desorption/ ture, the use of molecular typing in food-
become the genotypic method of choice ionization-time of flight (MALDI-TOF) borne disease investigations will assist us
for many scientists because it is very dis- mass spectrometry in identifying the source of many more
criminating, reproducible and broadly • pyrolysis (Py), outbreaks, will lead to the earlier detection
applicable. PFGE has recently been used • gas or liquid chromatography (GC of outbreaks, and will be beneficial in
to help in the investigations of wide- or LC), and identifying and eliminating areas of per-
spread foodborne outbreaks involving • infrared spectroscopy (IR). sistent contamination in food plants.


Next Steps in Food Safety Management
Foodborne illness in the United States approach to food safety will require that fewest cases of illness (approximately 50
the education of food safety profession- cases each) (Mead et al., 1999).
is a major and complex problem that is
als become more multidisciplinary. With the large number of pathogens
likely to become a greater problem as These broadly educated professionals responsible for foodborne illnesses and
we become a more global society. To will work in partnership with a wide the apparent lack of a single, all encom-
range of experts across government, in- passing solution to foodborne disease,
adequately address this complex
dustry and academia. how should a public health organization
problem, we need to develop and To achieve the maximum benefits, determine its priorities and distribute its
implement a well conceived strategic our food safety efforts and policies must resources to have the greatest impact on
be carefully prioritized, both in terms of food safety? The reality is that public
approach that quickly and accurately research and in application of controls. health priorities have always been influ-
identifies hazards, ranks the hazards by As scientific advances provide a better enced by a crisis like a recent outbreak or
level of importance, and identifies picture of pathogenicity, we must decide by the concerns of special interest
whether to focus our efforts on those groups. However, as a society, we need to
approaches that have the greatest pathogens that cause many cases of balance these influences with a more sys-
impact on reducing hazards, including moderate illness or instead focus on tematic approach that allocates scarce re-
those pathogens with the greatest severi- sources to have the greatest impact on
strategies to address emerging hazards
ty, despite the relatively few number of food safety.
that were previously unrecognized. cases. In the move toward making deci- Instead, a more strategic approach is
Because certain elements of patho- sions based on risk, our food safety poli- needed. Ranking hazards based on quan-
gen evolution are inherently unpredict- cies need to weigh these issues, and com- titative hazard analysis—to identify, in
able, it is impossible to predict, with ab- municate information about risk to all order of importance, those pathogens of
solute accuracy, the emerging microbio- stakeholders, including the public. principal concern to public health—pro-
logical food safety issues of the future. vides a scientifically based approach for
However, our knowledge of the current Strategic Prioritization to Reduce resource allocation. Criteria for such
issues and the complex factors that drive Foodborne Disease hazard ranking must be established. Ex-
changes in microbiological food safety amples of suitable criteria include: inci-
do provide us with a good sense of likely In an ideal world, gaps in data would dence and severity of illnesses, number
trends. With this knowledge and under- be quickly filled by data from high quali- and predisposing conditions of high-risk
standing, we can target our research and ty research. In reality, our research needs populations, principal risk factors asso-
surveillance efforts to spot emerging is- are far greater than our willingness to ciated with illness, and prevalence and
sues as they arise and be prepared to re- fund research. To maximize our resourc- virulence of the pathogen.
spond quickly and appropriately. Such a es, prioritization of research is essential. Efforts to prioritize public health-
response requires a flexible regulatory Similarly, our efforts at control and pre- problems based on more objective crite-
framework that is based on science. vention should focus first on areas with ria have been conducted in the past and
Recent scientific advances have pro- the greatest impact on public health. may serve as a model for food safety
vided tremendous insight into each of (Murray and Lopez, 1996).
the three factors in foodborne illness, Resource Priorities Difficulties exist, however, in weigh-
both separately and in combination. ing various components of public health
Knowledge of the pathogens themselves The Centers for Disease Control and impact when conducting quantitative
and their interaction with the microbial Prevention (CDC) estimates that 76 mil- hazard analysis for ranking pathogens.
environment creates opportunities for lion cases of foodborne illness occur an- For example, Salmonella species are re-
both prevention and control. Foodborne nually in the United States. A large num- sponsible for an estimated 1.34 million
illness surveillance systems can benefit ber of known pathogens are responsible cases of illness and 553 deaths, with a
from enhanced understanding of patho- for 14 million cases; for the other 62 mil- mortality rate of 0.04%, via a variety of
gen evolution to spot new problems lion cases, the pathogen causing the ill- foods of animal and plant origin. Most
quickly, and, in turn, the outbreak inves- ness is not known. Of the known patho- cases involve mild diarrhea of only a few
tigation data can provide further insight gens, Norwalk-like viruses (9,280,000 days duration. The young and elderly
into the forces that drive pathogen evolu- cases), Campylobacter species (1,963,000 populations are at greatest risk for severe
tion. Policies based on risk assessment cases), and nontyphoid Salmonella symptoms. On the other hand, V. vulnifi-
and Food Safety Objectives (FSOs) will (1,332,000 cases) are responsible for cus causes an estimated 47 cases of food-
enable us to better consider the impact of most illness, while Trichinella spiralis, borne illness and 18 deaths annually,
changing population demographics and Vibrio cholerae, and Vibrio vulnificus are principally via raw oysters. Forty percent
consumer behaviors. This science-based the known pathogens responsible for the of the cases involve fulminating septice-

mia that results in death. The population proach to develop critical food safety in- mal agriculture present a challenge. Cat-
at greatest risk is people with high levels of formation regarding the control of patho- tle, hogs, chickens and turkey produced
serum iron. These two very different food- gens in specific foods. For example, risk an estimated 1.37 billion tons of ma-
borne diseases illustrate the many factors assessments of Salmonella Enteritidis in nure in 1997 (U.S. Senate Agriculture
that must be considered in prioritizing the eggs, Escherichia coli O157:H7 in ground Committee, 1998). Because many of the
hazard ranking. Severity of illness, while beef, V. parahaemolyticus in raw mollus- most prominent foodborne pathogens
important, may or may not be the most can shellfish, and Listeria monocytogenes in the United States, including C. jejuni,
important factor in the ranking. in ready-to-eat (RTE) foods have been Salmonella, and E. coli O157:H7, are
Each agent responsible for foodborne drafted. When sufficient data are avail- carried by livestock and are principally
illness has unique characteristics that in- able, quantitative risk assessments can: transmitted to foods by fecal contami-
fluence its transmission or ability to cause identify what foods are of greatest risk nation, the amount of manure created
illness (Doyle et al., 1997). Transmission and contribute most to specific foodborne in the United States is a growing envi-
of Norwalk-like viruses is controlled by illnesses, estimate the levels of pathogens ronmental threat.
preventing contamination of food by hu- in foods that are unsafe, and identify what Manure-related food safety issues
man feces, whereas transmission of points within the food continuum have on the near term horizon include issues
Campylobacter jejuni is often controlled the greatest influence on exacerbating or related to fresh produce and organic
by preventing contamination of carcasses preventing foodborne illnesses. produce in particular. For example, re-
by poultry feces. Because there are so Examples of the use of case-control cent outbreaks of E. coli O157:H7 infec-
many different factors influencing patho- studies to identify risk factors for spo- tion and salmonellosis have been asso-
gen contamination of foods, no single so- radic illnesses include E. coli O157:H7, ciated with organically produced alfalfa
lution can be broadly applied to eliminate Campylobacter, and Cryptosporidium. and clover sprouts and mesclun lettuce.
foodborne illness; each agent must be ad- Major risk factors associated with spo- Use of contaminated cow manure is a
dressed on an individual basis with differ- radic cases of E. coli O157:H7 infection major concern. The lack of an estab-
ent procedures for control applied de- in the United States are eating under- lished, proven composting protocol to
pending on the pathogen. cooked ground beef and visiting a farm. assure elimination of pathogens and
Creating such a policy framework Risk factors for E. coli O157:H7 infection prevent recontamination contributes to
will not be an easy task. Tailored regula- in Scotland are handling/preparing raw this concern. Another issue on the hori-
tory responses that react to newly recog- food (40%), being involved in garden- zon is the importation of fruits and veg-
nized hazards with the best science avail- ing/garden play (36%), living on or visit- etables from countries with poor agri-
able at the time may be criticized as pre- ing a farm (20%), having direct/indirect cultural practices, i.e., use of contami-
mature or arbitrary regulatory enforce- contact with animal manure (17%), hav- nated irrigation water, improper prepa-
ment that creates uneven economic bur- ing private water supplies (12%), and re- ration and application of manure as fer-
dens within the food industry. But the al- cent failures with high coliform counts tilizer, and harvesting and washing pro-
ternative is waiting until there is signifi- of water supplies (12%) (Coia et al., duce under unsanitary conditions.
cant scientific information and applying 1998). Risk factors for sporadic Campy- Food irradiation has received con-
it in a uniform manner to all foods, lobacter infections in the United States, siderable attention as a means to ad-
whether they pose public health hazards identified in a case-control study of six dress food safety issues. The suggestion,
or not. Although this approach may be FoodNet sites from January 1998 however, that irradiation is a single so-
politically easier, it fails to maximize through March 1999 involving 1,463 pa- lution to eliminating most pathogens
public health protection. tients with Campylobacter infection and associated with fresh or RTE foods lacks
1,317 controls included: foreign travel, foundation. For some foods, irradiation
Strategic Control Measures eating undercooked poultry, eating results in foods with unacceptable sen-
chicken or turkey cooked outside the sory characteristics (Olson, 1998). Irra-
Because each pathogen must be ad- home, eating non-poultry meat cooked diation is a tool with broad applicability,
dressed individually, a strategic approach outside the home, eating raw seafood, but it is not a comprehensive solution
to applying control measures is neces- drinking raw milk, living on or visiting a for all infectious foodborne hazards in
sary. Within a strategic approach, inter- farm, contact with farm animals, and all foods.
vention strategies identify points at contact with puppies (Friedman et al.,
which control measures will have the 2000). Risk factors associated with Emerging Pathogens
greatest influence on providing safe cryptosporidiosis cases in Minnesota
foods. To identify and rank these points, from July 1-December 31, 1998, were Unfortunately, pathogens can be ad-
microbial risk assessments are conduct- swimming in public pools (e.g., hotel or dressed only after they evolve. Consider,
ed. The risk assessments involve system- school pools), drinking well water, visit- for example, the relatively recent identi-
atically collecting and analyzing expo- ing a farm, living on a farm for those less fication of E. coli O157:H7. E. coli
sure and dose-response data. Case-con- than age 6, and exposure to cattle and to O157:H7 received relatively little atten-
trol studies and other epidemiologic re- manure for those not living on a farm tion from food safety scientists and the
search approaches are helpful in identify- (Soderlund et al., 2000). The underlying medical community for more than a de-
ing risk factors in sporadic infections vehicle largely responsible for transmit- cade after its discovery. It was not until
and outbreaks. ting these pathogens to humans is con- 1993, following a large outbreak involv-
The U.S. Department of Agriculture taminated manure. ing more than 700 patients infected by
(USDA) and the Food and Drug Admin- The vast quantities of manure pro- eating undercooked fast-food hamburg-
istration (FDA) have used this general ap- duced each year as a by-product of ani- ers, that this pathogen rose to promi-


nence as a major food safety issue (Doyle mon pathogens, such as Salmonella Ty- lance programs. The core components
et al., 1997). USDA established a “zero phimurium (Bender et al., 2001). Rou- required for outbreak investigations in-
tolerance” policy for E. coli O157:H7 in tine subtyping and transmission of sub- clude: epidemiology, food protection
ground beef, the first rule to “outlaw” the type patterns through electronic com- programs, and public health laborato-
presence of a pathogen in a raw food munication networks, such as PulseNet, ries. The essential element to improving
(Griffin, 1998). Although some im- creates the potential to detect widely dis- foodborne outbreak investigations is the
provement has been made, the policy persed outbreaks that might not be rec- capacity to respond quickly and compre-
clearly has not resolved the problem, as ognized in any individual state (Swami- hensively to the occurrence of suspected
illnesses associated with ground beef nathan et al., 2001). Investigation of foodborne illness.
continue to occur. An estimated 73,500 these outbreaks is required to determine
cases of E. coli O157:H7 infection (both the source and mode of transmission of National Initiatives
food- and nonfood-related) occur annu- the outbreak-associated strain.
ally in the United States. Many outbreaks In addition to detecting outbreaks Foodborne illness has no easy solu-
are associated with swimming in recre- through laboratory-based surveillance, tions. However, major strides can be
ational lakes, drinking contaminated wa- outbreaks may also be recognized be- made by developing and implementing a
ter, handling animals, and consuming cause of the occurrence of similar ill- well-conceived strategic approach that
contaminated foods, including alfalfa nesses among persons who attended an prioritizes the hazards and defines the
sprouts, lettuce, unpasteurized apple event or establishment together. Many of strategies that will most effectively reduce
juice, coleslaw, and undercooked ground these outbreaks are recognized before a hazards. This approach must include a
beef (Doyle et al., 1997; Griffin, 1998). causative agent has been diagnosed. strategy to address emerging hazards.
Although the emergence of foodborne Thus, investigation of these outbreaks This strategic approach should be a na-
pathogens similar to E. coli O157:H7 can- must be conducted to identify the agent tional initiative that includes state, local,
not be anticipated, a well-conceived plan as well as the source and mode of trans- and international involvement, and per-
should be in place to address these issues mission. haps reorganizes existing federal food
as they arise. Essential information need- Outbreak investigations require the safety agencies and programs.
ed to assess the significance and likely im- close collaboration of epidemiologists, The importance of an expanded sur-
pact of the pathogen as an agent of food- environmental health specialists and pub- veillance system that covers animal
borne disease is often unavailable for a lic health laboratories. Collection of stool health and the environment cannot be
hazard analysis. Scientists need to know samples and interviews of ill persons and overstated. The additional information
the pathogen’s reservoir, prevalence, viru- healthy comparison groups must be con- from an expanded and coordinated sur-
lence, ability to survive in different envi- ducted rapidly. Epidemiologists must co- veillance system would enable a broader
ronments, and association with human ordinate their activities with the public vision of the flow of pathogens and po-
illness. Also, sensitive methods to detect health laboratories to maximize the po- tential pathogens throughout the food
the pathogen are often lacking. A frame- tential to isolate the agent. Information chain, and it would fill some important
work is needed to identify and prioritize collected by epidemiologists can help data gaps in risk assessment. Coupled
the information required for a hazard guide environmental health evaluation of with the new genetic tools, potential
analysis and a subsequent quantitative an establishment and interviews of food foodborne pathogens may be detected
microbial risk assessment. Public health service workers. Results of environmental before they cause confirmed human ill-
agencies should be prepared to quickly health evaluations can further guide epi- ness. While it may be politically or eco-
obtain the essential information to com- demiologic investigations. Epidemiologic nomically impractical to respond vigor-
plete a hazard analysis and, depending on data need to be analyzed and interpreted ously to a likely pathogen before cases
the degree of hazard and available data, a in light of the results of laboratory tests are identified and linked to the food/
risk assessment. and environmental investigations. Strate- pathogen combination, prior knowledge
gies for outbreak control and prevention of the potential pathogen will decrease
Outbreak Investigation need to be identified and implemented as response time and enable a more appro-
soon as can be justified by the results of priate first response. Expanded surveil-
A comprehensive system of food- the investigation. Depending on the scope lance will require state and local partici-
borne disease surveillance must include of the outbreak and nature of the re- pation, coupled with leadership and co-
a system for detecting and rapidly re- sponse, coordination with other state and ordination at the national level. Thus, ex-
sponding to potential outbreaks. Out- local agencies, FDA, USDA, and CDC panded surveillance should be part of
breaks caused by specific foodborne may be needed. any national initiative. These activities
pathogens, such as Salmonella and E. coli Most outbreak investigations are ini- also are consistent with international ef-
O157:H7, may be identified by detecting tiated by local or state health depart- forts being planned by the World Health
unusual case clusters or increased occur- ments. Because outbreak investigations Organization (WHO) towards establish-
rence of cases by routine surveillance of are complex activities that need to be ing a coordinated, expanded, worldwide
cases reported by medical clinics and rapid, thorough, and well-coordinated, surveillance system (Archer, 2001).
clinical laboratories. Recently, molecular CDC issued a report (CDC/NCID/
subtyping of isolates by pulsed-field gel DBMC, 2000) intended to assist state Strategies for the Future
electrophoresis (PFGE) has increased and local health departments assess their
both the sensitivity and specificity of outbreak response capacities and to help The complex interrelationship of the
pathogen-specific surveillance for detect- guide them in developing and strength- pathogen, host, and microbial ecology
ing outbreaks caused by relatively com- ening their foodborne disease surveil- ensures a role for everyone in food safety

management: government, industry, found to access data from food manu- pathogens, spotting new transmission
and consumers. A flexible, science- facturers. This is far from simple under patterns, or predicting the effects of new
based approach that relies on all parties current conditions. From their own production technologies.
to fulfill their role is our best weapon quality assurance (in-line, and environ- Pre-harvest Safety. In the last 10
against emerging microbiological food mental) and/or finished product moni- years, several teams have been formed to
safety issues. toring programs, manufacturers gather focus on the microbiological aspects of
huge amounts of data. If they were avail- pre-harvest food safety. These teams
Role of Government and Industry able, these data could provide valuable typically address animal production but
exposure information to risk assessors recently have also targeted produce. The
Developing a strategic, science-based and information on the prevalence of main emphasis of these teams has been
approach that prioritizes our resources pathogens in various food processing en- to define the existing problems, typically
will not be an easy task. Quantitative risk vironments. Food manufacturers cur- with the use of epidemiologic surveys,
assessment must be based on data, but rently do not often share such data or and to then develop and test intervention
our current system does not effectively even collect potentially useful informa- strategies. A good example is the efforts
encourage data generation and sharing. tion, because of potential regulatory to develop pre-harvest interventions for
The regulatory framework must be struc- ramifications or for product liability rea- E. coli O157:H7 in the beef production
tured to allow the food industry to gener- sons. Ways must be found to collect and industry. Such teams usually comprise
ate and share data and information with share this information in a penalty-free veterinary microbiologists, veterinarians,
the regulatory agencies. In addition, a sci- manner. food microbiologists, animal scientists,
ence-based program will necessarily in- For example, food producers con- and epidemiologists. The studies usually
volve acceptance of some level of risk, be- cerned with L. monocytogenes are hesi- use epidemiologic surveillance methods
cause zero risk is not achievable. Using the tant to test below the genus level, such to identify potential intervention points
FSO approach will enable us to translate that data show only Listeria spp. While in current animal production methods.
our public health goals into achievable somewhat useful, further speciation and These systematically designed studies
standards that are based on science. subtyping could yield even more useful generate large microbial strain sets. Cur-
Addressing consumer attitudes will data, but the finding of L. monocytogenes rently, these strains are often logged and
present a substantial challenge. Natural- in a finished, RTE food would result in stored, without generating much addi-
ly, we all desire the minimum possible regulatory action under current policy of tional data, save for occasional heroic ef-
risk that can be reasonably achieved. both FDA and USDA. Knowing how the forts to perform modest genotyping
Achieving consensus on an appropriate presence of other Listeria species in food studies. However, such strain sets and
level of risk will be difficult. Risk com- or the processing environment relates to the associated samples hold much infor-
munication and modification of percep- the possible presence of L. monocytogenes mation about the impact of different fac-
tion and behavior will need to be consid- is thus not achievable. tors on populations of pathogens and
ered an important part of any move to a Recent studies question whether all commensal organisms. This informa-
risk-based food safety policy. subspecies of L. monocytogenes are viru- tion could be mined in collaboration
Food manufacturers must accept lent, or of equal virulence (Wiedmann et with population geneticists and genome
their role in microbiological food safety al., 1997). Perhaps this finding, when researchers to examine the relationships
and achieving public health goals. Rapid further developed, will help define more between microbial population land-
response to a new food safety issue may appropriate policies that foster collection scapes, genome evolution, and ecology.
require investing money for controls be- of good and meaningful data. Addition- Sanitation Assurance. Surveillance
fore the scientific data are complete. In ally, knowing that the presence of L. studies of pathogens and indicator or-
exchange for flexibility, food manufac- monocytogenes alone may not necessarily ganisms in food production facilities are
turers must be willing to work as part- mean the food is potentially harmful a part of industry sanitation programs.
ners with regulatory officials, sharing sci- may be an incentive to manufacturers to These programs are designed to identify
entific information and data to develop speciate further, and to apply methods in-house events, catching potential haz-
appropriate food safety policies. that determine or indicate virulence or ards before they develop or become es-
Developing and implementing these lack of virulence. tablished in the production line. A care-
new, risk-based policies will require food Interdisciplinary Research. A growing fully designed sampling regimen, cou-
safety professionals with a broad under- area in federal research funding has been pled with the appropriate statistical
standing of many scientific disciplines the formation of interdisciplinary teams methods for data mining, could provide
and subjects. Changes in how we educate to examine complex problems. This shift a tremendous amount of information
food safety professionals will ensure they from more traditional projects with a sin- regarding the nature of hazardous events
have the knowledge and the skills to gle researcher has reached all the major and the identification of previously un-
maximize the effectiveness of new tools federal funding agencies. Some of these known hazards. Moreover, inclusion of
and methods. new interdisciplinary programs have been high-throughput genome studies on
highly successful, most notably in the ar- populations of pathogens or indicator
Data Sharing and Cooperation eas of vaccine development, epidemiolog- organisms would again provide a wealth
ic surveillance, and genome sequencing. of added information regarding evolu-
For risk assessments that are be These different program structures have tion and ecology of microorganisms in
based on the best data available and created new paradigms for the generation food production settings. In this context,
translate into the soundest science-based and sharing of data that provide added combining information from several dif-
decisions possible, ways need to be benefit for detecting the emergence of ferent producers could provide public


A Cooperative
The responsiveness and coordinated California Department of Health
Approach to the efforts of our institutions are critical Services, issued a special local need
factors in understanding and gaining registration that allowed seeds to be
Safety of Sprouts control of an emerging food safety is- treated with 20,000 ppm calcium hy-
Outbreaks of foodborne illness sue. In the case of sprouts, federal and pochlorite to kill pathogens. Federal
associated with the consumption of state government agencies worked co- and state agencies issued consumer
raw vegetable sprouts are a recently operatively with industry and academic advisories to warn at-risk popula-
emerged food safety issue addressed sectors to respond. CDC and FDA met tions (children, elderly, and those
using a combination of industry and with sprout industry representatives in with compromised immune systems)
regulatory action. 1995 to discuss food safety concerns. In to avoid consumption of raw
Sprouts can harbor large popula- 1997, the National Advisory Committee sprouts. Also in 1998, the National
tions of microorganisms, because the on Microbiological Criteria for Foods Center for Food Safety and Toxicolo-
conditions used for sprouting seeds (NACMCF) was asked to review avail- gy, a food safety research consortium
also promote rapid microbial growth. able data and to formulate science- comprised of industry, FDA and aca-
If present on the seeds, pathogens based recommendations to enhance the demic participants, formed a Sprouts
grow to high levels. In the 1980s and safety of sprouts. Task Force to identify data gaps and
1990s, consumption of fresh, un- A 1998 public meeting gathered prioritize short-term research goals.
cooked vegetable sprouts became sprout suppliers and trade organiza- All of these activities, along with
popular, and commercial sprout sup- tions, consumer groups, academic re- the NACMCF report (1999), formed
pliers developed broad distribution search scientists, federal and state gov- the scientific underpinnings for regu-
systems. The number of reported ill- ernment research scientists, and public latory guidance (FDA, 1999) with rec-
nesses increased significantly. In health officials to discuss the current ommendations for the sprout indus-
1997-1998 alone, at least 7 docu- scientific data and possible food safety try that were based on the best avail-
mented outbreaks of Salmonella and strategies. At that meeting, participants able scientific information at the time.
E. coli O157:H7 infections were shared information about epidemiolog- To reduce safety risks associated with
caused by consumption of various ic and outbreak data, agricultural and sprouts, the guidance documents pro-
types of raw vegetable sprouts. One sprouting practices, pathogen detection moted the combined approaches of
of these outbreaks, which occurred in methodology, and disinfection and con- good agricultural and manufacturing
Japan, was the largest outbreak of E. trol measures. In that same year, the practices, seed disinfection, and rapid
coli O157:H7 ever recorded (Taormi- California Environmental Protection pathogen testing of spent irrigation
na et al., 1999). Agency, acting on a request from the water.

health officials with further information This new approach will focus on ment of the integrated graduate food
about geographic and other factors asso- preparation of professionals who, in ad- safety education programs that will pro-
ciated with the emergence and spread of dition to expertise in their primary disci- vide the larger, multidisciplinary work-
populations of problematic organisms. pline, also are grounded in supporting force needed to address emerging food
food safety areas such as veterinary, ag- safety issues.
Food Safety Education ronomic, environmental and public
health practices. Although it is difficult Role of Consumer Understanding
New integrative educational ap- for a single campus to provide such
proaches that directly link the basic and broad training, yet through creative col- For the last 30 years, the dominant
applied sciences will be necessary to ef- laborations, new food safety curricula al- food safety message has been that the
fectively train the future food safety pro- ready are developing. These programs United States has the world’s safest food
fessional. For instance, tomorrow’s food make aggressive use of distance learning supply. As a result, most consumers be-
safety professional must be knowledge- technologies; emphasize critical thinking lieve that there is in place an extensive
able in basic sciences such as microbiol- skills, professional development and eth- system of controls applied throughout
ogy and toxicology, yet also understand ics training; provide practical field expe- the food production and distribution
the entire food safety continuum and be rience through summer internships; and system, guaranteed ultimately by govern-
able to address issues wherever they oc- devote special attention to diversity is- ment oversight, and that this system pro-
cur along that continuum. And because sues to create a highly trained and well- tects them against well-recognized and
microbiology and toxicology are inti- represented work force (Jaykus and emerging foodborne disease. One of the
mately tied to newer disciplines such as Ward, 1999). Food science departments consequences of this confidence is that
molecular biology, genomic sciences, and around the country are uniquely posi- food safety problems may be seen only as
mathematical modeling, extensive sub- tioned to offer the strongest and most defects of the system to be fixed by
discipline training remains crucial. comprehensive leadership in the develop- strengthening the system of controls and

government action, rather than also as progress of education programs (Altek- recognizing that food safety is not only
problems with a strong component of ruse et al., 1999; Yang et al, 1998). Data the responsibility of the federal govern-
consumer-based risk reduction or risk collected through the Behavioral Risk ment, but is the shared responsibility of
avoidance. Factor Surveillance Systems during all components of the food system from
Studies indicate that 80% of con- 1995-1996, which included 19,356 sur- primary producers to consumers. Con-
sumers think food safety problems are vey participants, showed that several high sumer education about risk reduction
mainly due to failures in food process- risk food handling, preparation, and will be a valuable component of an FSO
ing, food distribution and food prepara- consumption behaviors were common, program. Consumers will need to under-
tion in restaurants; in other words, con- and some varied by gender, age, race/eth- stand their role in preventing foodborne
sumers believe the failures are occurring nicity, education and income. For exam- illness.
in the most regulated parts of the food ple, 50.2% of respondents reported eat- Numerous sources provide a wealth
safety system where they have little direct ing undercooked eggs, and 19.7% report- of information about food safety and
responsibility. Relatively few consumers ed eating undercooked hamburgers. All other food-related issues in many for-
perceive food safety problems due to ac- high risk food handling, preparation, mats to meet the needs of various audi-
tions in the home or in supermarkets— and consumption behaviors were more ences. Different information sources
the final stage of the food safety sys- prevalent in men than in women. The serve different needs, and the effective-
tem—or on farms—the beginning of the prevalence of reported consumption of ness is not equal.
system (Levy, 1997; Penner et al., 1985; undercooked hamburgers decreased with Consumer Information Sources. Sur-
Williamson, 1991). To achieve a truly age, increased with education, and in- veys indicate that people get most of their
farm-to-table approach to maximizing creased with income. information about food safety from elec-
food safety, it is important to consider Decisions about behavior frequently tronic and print news media; additional
potential contributions from all seg- are guided by risk perception rather than information sources include labels and
ments of the food chain. risk awareness (Frewer et al., 1994). De- food packages, regulatory agencies, and
Since 1993, the Food Marketing Insti- fining risk as “hazard + outrage,” Sand- cookbooks (Hingley, 1997; Levy, 1997).
tute Trends Survey has asked consumers man (1997) stated that when people mis- A national educational campaign of
an open-ended question about the great- perceive hazards it is often because they the Partnership for Food Safety Educa-
est threats to food safety to measure top of are outraged. Sandman noted that gen- tion (a public-private partnership of the
the mind awareness of different possible erally, even when the hazard is serious, federal government, food industry, and
sources of food safety problems. The the public is apathetic and the least dan- consumer organizations), FightBAC!TM,
number of respondents who mentioned gerous hazard often generates the great- was created in 1996 to conduct broad-
improper quality control/shipping/han- est outrage. He said, “Too often, experts based food safety education designed to
dling and storage rose from 9 percent in focus on the hazard and ignore the out- reach people of all ages. The FightBAC!TM
1993 to 34 percent in 1997. During the rage while the public focuses on the out- campaign has produced multiple educa-
same time period, the number of people rage and ignores the hazard.” Under tional tools used through many informa-
mentioning food preparation declined these circumstances, the hazard cannot tion channels, i.e., public service an-
from 12 percent to 2 percent. be mitigated without addressing their nouncements, the Internet, point of pur-
outrage. Sandman suggested that experts chase materials, and school and commu-
Consumer Behavior determine why the outrage is high and nity outreach.
what can be done to lower it so that peo- The National Food Safety Informa-
Research indicates that people con- ple want to hear or acknowledge the ex- tion Network formed in 1998 by FDA’s
sider themselves fairly knowledgeable tent of the hazard. As an example, Sand- Center for Food Safety and Applied Nu-
about food safety guidelines, and for the man stated that “consumers know how trition (CFSAN) and USDA’s Food Safe-
most part they are. However, as in other to cook and generally will get angry if ty Inspection Service (FSIS) and Na-
areas of health and safety, knowledge and you tell them how to do something they tional Agricultural Library reaches con-
awareness does not always translate into already know about.” sumers with information on food-relat-
behavioral changes. Between 1988 and If people do not recognize and accept ed issues and safe food handling via
1993, indicators of concern about food their role in food safety problems, behav- USDA’s Meat and Poultry Hotline, CF-
increased significantly, suggesting an ior change is unlikely. One way to break SAN’s Outreach Information Center,
emerging public awareness and interest through public misconceptions is to de- USDA/FDA’s Foodborne Illness Educa-
in food safety problems. At the same scribe the magnitude of food safety tional Information Center, the
time, data suggest that unsafe food con- problems and challenge people’s under- web site, EdNet (food
sumption and preparation behavior ac- standing of themselves as experts. New safety educators’ network), and the
tually increased (Levy, 1997). data from the FoodNet surveillance sys- Foodsafe listserve. Considered the
Behavioral surveillance systems can tem may be the best way to challenge “gateway to government food safety in-
provide data identifying people or people’s understanding of themselves as formation,” the web
groups in which behaviors associated experts (Levy, 1997). site provides the public access to advice
with foodborne diseases are more com- pertaining to specific population sub-
mon and who are at higher risk for food- Consumer Education groups (e.g., children, people with im-
borne illness, thus assisting in the devel- mune diseases) as well as product spe-
opment of food safety education pro- Recent federal initiatives have sought cific advice (e.g., refrigerated RTE
grams (Yang et al., 1998). Further, sur- to improve the safety of the U.S. food foods). CFSAN and FSIS also have con-
veillance data can be used to evaluate the supply using a farm-to-table approach, ducted public awareness campaigns.


For example, CFSAN developed materi- rate the effects of different forms of in- • the nature of the benefits (e.g., who
als (press kits, consumer brochure, vid- formation because consumers are ex- benefits and in what ways);
eo news release, and public service an- posed to several information sources si- • uncertainties in risk assessment (e.g.,
nouncement) explaining the risk that multaneously and information sources the methods used to assess the risk and
unpasteurized or untreated juices may may interact in their effect on percep- weaknesses in the available data); and
pose to vulnerable populations. The tions. The authors concluded that the • risk management options (e.g., ac-
materials were targeted to a variety of results show that consumers who are tion taken to control the risk and action
audiences (senior citizen groups, day more aware of risk from undercooked individuals may take to reduce personal
care centers, elementary schools, and hamburger are more likely to adopt safe risk) (FAO/WHO, 1998).
PTA offices). Similarly, FSIS launched a behavior and thus contribute to a re- A National Research Council Com-
“Thermy the Thermometer” campaign duction of foodborne disease. mittee on Risk Perception and Commu-
in 2000 to encourage use of thermome- nication (NRC, 1989) addressed ways to
ters to ensure sufficient cooking of meat Risk Communication improve risk communication. The com-
and poultry. mittee noted that it is a mistake to expect
Consumer Trust in Information. Risk communication is a necessary the public to always want simple answers
Consumers place different levels of and critical tool to appropriately define about risk; often, at least part of the pub-
trust in information from different issues and to produce the best risk man- lic desires considerable detailed informa-
sources. A survey of more than 1000 agement decisions (FAO/WHO, 1998). tion about risks. The committee con-
Americans conducted by the University Risk communication has been defined as cluded that successful risk communica-
of Kentucky found that more consum- the interactive exchange of information tion improves or increases the base of ac-
ers “completely trusted” the accuracy of and opinions concerning risk and risk curate information that decision makers
the information from government pub- management among risk assessors, risk use, whether they are government offi-
lications and food labels than from any managers, consumers and other interest- cials, industry managers, or individual
other source (Buzby and Ready, 1996). ed parties (CAC, 1997b). Others have citizens, and, at the same time, satisfies
Of those respondents who trusted food added risk-related factors to the defini- those involved that they are adequately
safety information from government tion, reflecting a wider risk communica- informed within the limits of available
publications, 10.8% trusted the accura- tion concept (FAO/WHO, 1998). knowledge. Further, the committee ex-
cy completely. Of those who trusted Several factors play a role in under- plained that because risk communica-
food safety information on food pack- standing and communicating risk: tion is tightly linked to the management
aging and labels, 10.2 percent did so whether a risk is voluntary or involun- of risks, solutions to the problems of risk
completely. Consumers’ complete trust tary, whether the distribution of risk communication often entail changes in
of store brochures and advertisements and benefit is equitable, the degree of risk management and risk analysis. In
was lower than other sources, 3% and personal control, the individual dread moving toward risk-based food safety
1.4% respectively. The authors stated of the adverse event, the catastrophic policies, risk communication with all in-
that it is not surprising that these were potential of the event, and the extent of terested parties, including risk assessors,
the least trusted of the seven sources of trust in the risk managers (Covello et risk managers, and the public, will be an
food-safety information, because people al., 1988; NRC, 1989; Sandman, 1987). important part of the process (NRC,
may feel that advertisers have incentives A Consultation of the Food and Agri- 1989).
to make positive claims about their cultural Organization (FAO) of the The FAO/WHO Consultation also
products. United Nations and WHO (FAO/WHO, identified several considerations for
Addressing the data on how compet- 1998) described these principles of risk framing risk communication strategies.
ing motivations, risk perception, and communication: (1) know the audience, From an international perspective, ad-
taste preferences affect hamburger prep- (2) involve the scientific experts, dressing the critical role of effective com-
aration, Ralston et al. (2000) reported (3) establish expertise in communica- munication in determining equivalence
that several information channels ap- tion, (4) be a credible source of infor- of food control measures in different
pear to be effective for communicating mation, (5) share responsibility, (6) dif- countries is a consideration. From an
the risks of unsafe food preparation. ferentiate between science and value industry perspective, labeling is a consid-
Respondents who said they get their in- judgment, (7) assure transparency, and eration. The consultation recommended
formation from magazines, television, (8) put the risk in perspective. Barriers that if consumer food handling, storage
cookbooks, or government hotlines had to effective risk communication can oc- or other practices can assist in control-
15-17% higher risk motivation, i.e., cur within the risk analysis process (e.g., ling a foodborne illness or disease out-
were more risk averse, than those who inadequate access to vital information break, clear instructions using unambig-
did not cite these sources of informa- and inadequate participation of inter- uous language should be presented. The
tion. Respondents who said that they ested parties) or in a broader context effectiveness of labeling as a risk man-
get information from labels did not (e.g., differing perceptions among par- agement/communication strategy, how-
have a higher risk motivation index af- ticipants, limited understanding of the ever, needs further study. The consulta-
ter accounting for other factors that also scientific process, lack of credibility of tion recommended that labeling—
increase awareness. Consumers who the information source, and societal which has been used extensively to con-
cited brochures as their information characteristics). Elements of effective vey information such as product com-
source had lower risk motivation than risk communication include: position, nutrition, weights and mea-
respondents who did not. Ralston et al. • the nature of the risk (e.g., its magni- sures, and health-related warnings—
(2000) noted that it is difficult to sepa- tude and severity); should not be used as a substitute for

consumer education. The consultation application of food safety measures systems. For example, treatment of a
also stated that because national gov- (FAO/WHO, 1998) and refers to Codex raw vegetable with a new chemical dis-
ernments are responsible for food quali- standards as international benchmarks infectant might eliminate concern over
ty and safety and are the primary sources for nations. certain pathogens of manure origin.
for risk communication with the public However, this treatment also might in-
on food safety issues, the capability to ef- Anticipating the Future: Food advertently select for unidentified mi-
fectively communicate risks should be Safety Issues on the Horizon croorganisms that were previously in-
one of the highest priorities for these consequential but that become hazard-
agencies. Looking ahead, and considering the ous without normal microbial competi-
It is important that risk communica- content of this report, several food safety tion to keep their numbers in check.
tion involve effective dialogue, a two-way issues are likely to come to the forefront The complex relationship between vari-
exchange, among interested parties in the next decade. ous factors cannot be overlooked.
(NRC, 1989). Effective dialogue goes be- Similarly, the introduction of any
yond passively providing access to the Globalization of the Food Supply novel food requires a full analysis to as-
risk message formation process, e.g., via sess the potential microbial hazards.
pro forma public hearings, to including FDA electronically screened all 2.7 The hazard analysis must be broad
early in the process all interested and af- million entries of imported foods under enough to consider all the intrinsic and
fected groups and comprehending the its jurisdiction in fiscal year 1997, and extrinsic conditions that influence
range of potentially contending view- physically inspected 1.7%, or 46,000 en- pathogens known to be associated with
points (NRC, 1989). tries. FSIS visually inspected all 118,000 foods, ingredients or processes related
Addressing the importance of broad entries of imported meat and poultry to the novel food being introduced. The
participation in communication of in- under its jurisdiction in calendar year analysis also must consider microor-
terested and affected parties, a National 1997, and conducted further physical ganisms unique to the new situation
Research Council (NRC) Committee on examination of about 20% of entries. that pose a threat to safety of the novel
Risk Characterization reported (NRC, These numbers of entries will only in- food.
1996) that deliberation is intimately crease in the future, and this brings into Similar considerations are essential
connected with and as important as question how the regulatory agencies with the introduction of any alternative
analysis in understanding risks. The will handle the increases most effective- technology or combination of various
committee stated that analysis and de- ly and efficiently. The shortcomings of alternative technologies and/or preser-
liberation can be thought of as two sampling and analysis for the ever in- vatives. It is essential to identify the
complementary approaches to gaining creasing list of pathogens, natural tox- pathogens that are most resistant to the
knowledge of the world, forming under- ins, or pesticide and industrial chemi- alternative technology, determine mech-
standings on the basis of knowledge cals suggest that different approaches anisms of inactivation or control in-
and reaching agreement among people. must be sought. HACCP is gaining rec- cluding required conditions and kinet-
Defined by the committee as any formal ognition worldwide as a desirable sys- ics, identify validation procedures, and
or informal process for communication tem of safety assurance, but for interna- describe critical process factors.
and for raising and collectively consid- tional trade, mutual recognition of Scientists continue to be challenged
ering issues, deliberation is important HACCP systems must be sought. to adequately address all the parameters
in risk decision-making for its role in The demand for year-round fresh associated with the introduction of a
considering conflicts of values and in- fruits and vegetables is firmly estab- novel food or alternative processing
terests. A variety of techniques are used lished in the United States. Again, the technology. Once developed, new tech-
for deliberation and public participa- volume of fresh produce being offered nologies must be appropriately regulat-
tion. These include citizen advisory for entry into the United States will only ed to ensure their proper application
committees and task forces, alternative continue to grow, as will the variety of and acceptance by the public.
dispute resolution, citizens juries and produce offered. Without mutual un-
panels, surveys, focus groups, interac- derstanding and application of good ag- Increases in Organic Foods
tive technology-based approaches, and ricultural practices, resulting in mutual
combinations of methods (NRC, 1996). recognition of systems to assure safety, Organic foods are becoming main-
Risk communication takes place at regulatory agencies will be further stream items in most grocery stores, and
local, national, and international levels. stressed. it is likely that this segment of the fresh
On an international scale, risk commu- produce industry will continue to grow.
nication on food safety occurs within Alternative Processing Technologies With or without facts to back up the as-
Codex Alimentarius Commission, its sumption, consumers assume organic
and Novel Foods
subsidiary bodies, and its United Nations produce is more nutritionally complete
parent organizations, FAO and WHO, Novel foods and alternative process- and safer than conventionally grown
and their expert advisory groups. The ing technologies will continue to appear. produce. Recent outbreaks of salmo-
Sanitary and Phytosanitary Measures With each new introduction, we must nellosis and E. coli O157:H7 infection
Agreement of the World Trade Organiza- consider the possible consequences, in- associated with organically produced
tion encourages harmonization and tended and unintended, within the food sprouts and mesclun lettuce grown and
places a strong emphasis on risk com- system. Some technologies will reduce distributed in the United States are evi-
munication principles of transparency or eliminate microbiological hazards in- dence of an emerging problem (Griffin,
and consistency in the development and herently present in current food safety 1998; Hilborn et al., 1999). Cow ma-


nure is a well-documented vehicle for as Salmonella. As people live longer, they lence, and even help determine why and
Salmonella and E. coli O157:H7, and its may develop more chronic underlying ill- what to do about it.
use in produce production must be nesses that predispose them to foodborne
controlled to prevent contamination. illness. Increasingly complex combina- Consumer Understanding
With an estimated 1.2 billion tons of tions of drugs to treat various conditions
manure produced by cattle annually in in the elderly can have unpredictable ef- Although consumers are only a small
the United States (U.S. Senate Agricul- fects on susceptibility. Formerly fatal con- part of the food safety chain, as consum-
ture Committee, 1998), this voluminous ditions, such as loss of major organ func- ers we all need to take responsibility for
source of foodborne pathogens is likely tion, are now survivable thanks to organ our contribution to food safety. Those
to be an influential factor in the trans- transplants. The numbers of transplant that have not already done so must ac-
mission of foodborne illness for the recipients will likely increase with time, cept that zero risk is not a reality. These
foreseeable future. Methods are needed but it is important to remember that these two concepts may be difficult for some
to reduce the shedding of pathogens in individuals may be among the most sus- consumers to accept. Education and risk
livestock and poultry and to identify ef- ceptible populations to certain foodborne communication will be necessary to pro-
fective procedures for eliminating pathogens. vide consumers with a more accurate
pathogens in manure before they con- perception of food safety risks and to en-
taminate the environment and food. Pathogen Evolution courage behavior modification, where
Changes in Food Consumption Microbial evolution has always hap-
pened and will always happen. Bacteria, Integrated Food Safety System
The global trade in food stuffs is only for example, have an enormous capacity
one force in people’s changing dietary for mutation, integration of new genetic A farm-to-table food safety system
patterns. Certainly the variety of avail- material, and recombination of genetic must involve many interested parties work-
able food has expanded drastically and material in order to assure survival. Bac- ing together toward a common goal. When
will continue to do so. Ethnic foods are teria can sense and react to their envi- properly applied, the FSO approach would
increasingly popular, and the percentage ronment and genetically change them- incorporate input from all stakeholders in
of foods prepared and/or consumed out- selves in response. Unfortunately, newly developing the appropriate levels of protec-
side the home will continue to rise. Fruits evolved pathogens are first recognized tion. Although regulatory oversight is nec-
and vegetables are likely to constitute a when they cause an outbreak of illness. essary to monitor and enforce the perfor-
greater portion of the average diet, and Using new technologies and genomics, mance of the food safety system, food
the consumer demand for “fresh” prod- perhaps surveillance of food animals manufacturers must play an important
ucts will lead to more minimally pro- and the environment for newly emerging role as well, because they have first-hand
cessed foods. Our control and preven- microorganisms with pathogenic poten- information about food safety hazards and
tion methods will need to be adapted to tial will become a reality in the future, the production environment. A partner-
these changing dynamics. and there will be no need to wait for hu- ship environment will enhance data shar-
man illness. Another hope for the future ing and provide a solid scientific basis for
At-Risk Subpopulations is a better understanding of how human policies. An ideal system identifies hazards,
activities affect foodborne pathogens. institutes appropriate controls in a flexible
It is likely that the number of persons For example, does the cross protection manner through FSOs, and monitors the
at higher risk for foodborne disease afforded a pathogen by exposure to an operation of the system. The challenge is to
agents will continue to increase with time. environmental insult have a negative im- build a system that applies science in a pre-
The population of the United States is ag- pact on further processing? Genomics dictable, consistent, and transparent man-
ing, and clearly aging is a risk factor for may also provide a better snapshot of ner to enable harmonization within and
more serious outcomes from agents such how a microorganism manifests viru- between countries.

History has demonstrated that science, commercial canning of low acid foods. (HACCP) systems, continue to be
when appropriately applied through Our current level of food safety is the refined as we strive to further improve
food safety management policies, can result of effective implementation on food safety.
dramatically improve food safety. The the part of industry, government, and This report articulates the science be-
past century produced numerous consumers. More recent approaches, hind microbiological food safety, espe-
cially as it relates to emerging microbio-
examples: refrigeration of perishable such as the development of Hazard logical hazards. Interpretation and anal-
foods, pasteurization of milk, and Analysis and Critical Control Point ysis of this scientific information pro-

nure is a well-documented vehicle for as Salmonella. As people live longer, they lence, and even help determine why and
Salmonella and E. coli O157:H7, and its may develop more chronic underlying ill- what to do about it.
use in produce production must be nesses that predispose them to foodborne
controlled to prevent contamination. illness. Increasingly complex combina- Consumer Understanding
With an estimated 1.2 billion tons of tions of drugs to treat various conditions
manure produced by cattle annually in in the elderly can have unpredictable ef- Although consumers are only a small
the United States (U.S. Senate Agricul- fects on susceptibility. Formerly fatal con- part of the food safety chain, as consum-
ture Committee, 1998), this voluminous ditions, such as loss of major organ func- ers we all need to take responsibility for
source of foodborne pathogens is likely tion, are now survivable thanks to organ our contribution to food safety. Those
to be an influential factor in the trans- transplants. The numbers of transplant that have not already done so must ac-
mission of foodborne illness for the recipients will likely increase with time, cept that zero risk is not a reality. These
foreseeable future. Methods are needed but it is important to remember that these two concepts may be difficult for some
to reduce the shedding of pathogens in individuals may be among the most sus- consumers to accept. Education and risk
livestock and poultry and to identify ef- ceptible populations to certain foodborne communication will be necessary to pro-
fective procedures for eliminating pathogens. vide consumers with a more accurate
pathogens in manure before they con- perception of food safety risks and to en-
taminate the environment and food. Pathogen Evolution courage behavior modification, where
Changes in Food Consumption Microbial evolution has always hap-
pened and will always happen. Bacteria, Integrated Food Safety System
The global trade in food stuffs is only for example, have an enormous capacity
one force in people’s changing dietary for mutation, integration of new genetic A farm-to-table food safety system
patterns. Certainly the variety of avail- material, and recombination of genetic must involve many interested parties work-
able food has expanded drastically and material in order to assure survival. Bac- ing together toward a common goal. When
will continue to do so. Ethnic foods are teria can sense and react to their envi- properly applied, the FSO approach would
increasingly popular, and the percentage ronment and genetically change them- incorporate input from all stakeholders in
of foods prepared and/or consumed out- selves in response. Unfortunately, newly developing the appropriate levels of protec-
side the home will continue to rise. Fruits evolved pathogens are first recognized tion. Although regulatory oversight is nec-
and vegetables are likely to constitute a when they cause an outbreak of illness. essary to monitor and enforce the perfor-
greater portion of the average diet, and Using new technologies and genomics, mance of the food safety system, food
the consumer demand for “fresh” prod- perhaps surveillance of food animals manufacturers must play an important
ucts will lead to more minimally pro- and the environment for newly emerging role as well, because they have first-hand
cessed foods. Our control and preven- microorganisms with pathogenic poten- information about food safety hazards and
tion methods will need to be adapted to tial will become a reality in the future, the production environment. A partner-
these changing dynamics. and there will be no need to wait for hu- ship environment will enhance data shar-
man illness. Another hope for the future ing and provide a solid scientific basis for
At-Risk Subpopulations is a better understanding of how human policies. An ideal system identifies hazards,
activities affect foodborne pathogens. institutes appropriate controls in a flexible
It is likely that the number of persons For example, does the cross protection manner through FSOs, and monitors the
at higher risk for foodborne disease afforded a pathogen by exposure to an operation of the system. The challenge is to
agents will continue to increase with time. environmental insult have a negative im- build a system that applies science in a pre-
The population of the United States is ag- pact on further processing? Genomics dictable, consistent, and transparent man-
ing, and clearly aging is a risk factor for may also provide a better snapshot of ner to enable harmonization within and
more serious outcomes from agents such how a microorganism manifests viru- between countries.

History has demonstrated that science, commercial canning of low acid foods. (HACCP) systems, continue to be
when appropriately applied through Our current level of food safety is the refined as we strive to further improve
food safety management policies, can result of effective implementation on food safety.
dramatically improve food safety. The the part of industry, government, and This report articulates the science be-
past century produced numerous consumers. More recent approaches, hind microbiological food safety, espe-
cially as it relates to emerging microbio-
examples: refrigeration of perishable such as the development of Hazard logical hazards. Interpretation and anal-
foods, pasteurization of milk, and Analysis and Critical Control Point ysis of this scientific information pro-

vides insight into food safety policies foodborne disease; (3) improve control on name, serotype or other traits unre-
and management practices. At the sim- strategies; and (4) monitor trends in oc- lated to virulence. This research will
plest level, foodborne illness can be re- currence of foodborne disease. Com- improve our evaluation of safety, which
duced to three factors: the pathogen, the prehensive, coordinated surveillance ac- currently is focused on microbes that
host, and the environment in which they tivities must be expanded to include an- may or may not be pathogenic.
interact. Any efforts to improve food imal health and the production and Recent advances in genomics have
safety must address these factors. processing environment. Integrating contributed to the further understand-
Managing microbiological food animal and environmental surveillance ing of virulence at the genus level (e.g.,
safety is a complex task. Microbiological systems into established human surveil- Salmonella) and at the level of specific
hazards are ever-changing, and the lance systems will greatly increase our strains within a species (e.g., Escheri-
amount and complexity of data and the understanding of the epidemiology and chia coli O157:H7). Genomics also has
residual unknowns are growing at a sources of foodborne disease. greatly facilitated our understanding of
rapid rate. Each new scientific advance Enhanced surveillance will provide the continuous and sometimes rapid
gives us the opportunity to add to our data that can be used in risk assessment, evolution of pathogens.
knowledge of foodborne illness using which is appropriately becoming a Adverse changes in the microbial
new techniques and researching new foundation for selecting food safety environment and ecology may cause
questions. At the same time, human management options. One of the pri- bacteria to experience stress. Although
susceptibilities are increasing, and our mary limiting factors for quantitative many bacteria die, some may survive,
ability to link food to adverse health risk assessment is the quality and suffi- because bacteria have elaborate systems
outcomes is improving. The human ciency of available data. As an example, to adapt to environmental stress. In ad-
health and economic consequences of there is little information available dition to tolerance of the original
emerging microbiological food safety is- about the relationship between the stress, the surviving microorganisms
sues are immense. To address these cir- quantity of pathogen ingested and re- also may be tolerant to other unrelated
cumstances, food safety policies should sulting frequency and severity of ad- stresses, and these tolerant microor-
be developed as part of national initia- verse health effects, especially for sus- ganisms may demonstrate increased
tives, with input from all stakeholders. ceptible subpopulations. Risk assess- virulence. Understanding these re-
International coordination of food ment is an iterative process, and assess- sponse mechanisms will provide the
safety efforts should be encouraged. ments must be updated as additional information necessary to refine food
Globalization of the food supply has information becomes available. As risk processing conditions or to develop
contributed to changing patterns of assessments are refined with better other appropriate intervention strate-
food consumption and foodborne ill- methods and improved data, their new gies that enhance food safety.
ness. Global food trade has the poten- conclusions must be shared broadly Improved analytical systems are
tial to introduce pathogens to new geo- with all stakeholders to enlighten the needed to gather better data about
graphic areas. In addition, we have gen- public debate over appropriate levels of pathogens in the food production envi-
erally less knowledge about the growing protection. ronment to improve our understand-
conditions and processing and distribu- Our scientific understanding of the ing of the microbial ecology in these
tion practices for imported foods than microbiology of foodborne pathogens situations. Sensitive quantitative meth-
for foods produced domestically. continues to improve. Scientists are ods are necessary for assessing patho-
Scientific research has resulted in only just beginning to understand the gen growth, survival, and inactivation,
significant success in improving food factors that cause a particular microbial as well as for accurate risk assessments.
safety, but the current science underpin- strain to be pathogenic while other New processing and packaging
ning the safety of our food supply is not strains of the same microorganism are technologies offer the potential for
sufficient to protect us from all the not, the ways by which some microor- continued improvement in the organo-
emerging issues associated with the ganisms adapt and evolve to become leptic quality of foods, extended shelf
complexity of the food supply. The body pathogenic, and the mechanisms patho- life, and enhanced microbiological
of scientific knowledge must be further gens employ to adapt to differing envi- safety. However, these new processes
developed, with our research efforts ronments. Further research is essential and packaging technologies may
carefully prioritized to yield the greatest to understand microbial ecology and change the microbial ecology, resulting
benefit. Food safety and regulatory poli- virulence sufficiently well to anticipate in potential positive and negative ef-
cies must be based on science and must future microbial hazards and construct fects that must be assessed along the
be applied in a flexible manner to incor- barriers to disease. entire food chain. Even an apparently
porate new information as it becomes Some pathogenic microorganisms insignificant change in the microbial
available and to implement new tech- are significantly more virulent than oth- environment can trigger a food safety
nologies quickly. The food industry, ers. Virulence may vary within species, concern because of the complexity of
regulatory agencies and allied profes- subspecies, and even different strains. the microbial environment and the in-
sionals should develop partnerships to Understanding the many different viru- terrelationship of various factors.
improve food safety management. lence factors that microorganisms use Combinations of food manufactur-
Human foodborne disease surveil- to cause illness offers opportunities to ers’ efforts, regulatory programs, and
lance will continue to be very important develop better controls and therapeu- consumer actions have driven down
to: (1) identify outbreaks of foodborne tics. Further research will enable scien- rates of certain foodborne diseases, but
disease so they can be controlled and tists to classify pathogens based on spe- continued efforts are necessary. Al-
prevented; (2) determine the causes of cific virulence factors rather than based though not easy to accomplish, it is


critically important that regulatory pol- residual levels of pathogens will be food is consumed. FSOs would enable
icies be based on the best science cur- more likely to achieve public health food manufacturers to design processes
rently available. Regulatory policies goals than policies that haphazardly in- that provide the appropriate level of
based on sampling and testing may in- terdict some small percentage of con- control and that could be monitored to
correctly imply an absence of patho- taminated produce. verify effectiveness. Establishing FSOs is
gens, causing some individuals to as- Although a great deal of progress a societal issue that will require inclu-
sume that it is unnecessary to engage in has been made in minimizing contami- sive participation of all sectors of soci-
proper food selection and handling nation of animal carcasses during ety.
practices. Given the characteristics of slaughter, the occasional presence of The FSO approach can be used to
some foods, available technologies, and pathogens on meat and poultry carcass- integrate risk assessment and current
our desire for year-round availability of es is largely unavoidable. Prescribed hazard management practices into a
a diverse array of foods, it is unlikely microbial control processes and regula- framework that achieves public health
that the marketplace can be made free tory standards—in combination with a goals in a science-based, flexible man-
from the presence of pathogenic micro- number of other important risk-reduc- ner. FSOs help translate the outcome of
organisms at all times. ing measures, including educational risk assessment into something that can
The large-scale production of some programs—apparently have minimized be used with HACCP programs. The
ready-to-eat (RTE) foods consistently the risk of E. coli O157:H7 infections. FSO approach will be successful when
free of Listeria monocytogenes appears Some segments of the marketplace are directly intertwined with a food proces-
practically impossible. A great deal of successfully using strict purchase speci- sor’s good manufacturing practices
progress has been made during the past fications as part of sophisticated quality (GMPs) and HACCP systems.
quarter century to reduce the levels and control programs. Unfortunately, this Although HACCP is a science-based
frequency of contamination of ready- combination of factors is not in place management tool, HACCP may not be
to-eat foods during their manufacture, for all parts of the marketplace. Con- an appropriate approach for all circum-
but consistently assuring the absence of tinuing to focus on “limit-of-detection stances. It is not possible to have a valid
Listeria has remained out of reach. This pathogen standards” for some raw HACCP plan when a scientific analysis
bacterium is commonly present in the meats in the absence of effective mea- does not identify any point that meets
environment and is constantly reintro- sures in other parts of the farm-to-table the critical control point criteria. HAC-
duced into the processing environment continuum is more likely to shift the CP implementation must remain flexi-
on raw ingredients and via other means. risk to other parts of the marketplace ble to incorporate the scientific knowl-
Listeria survives well in the manufactur- (such as those with less strict purchase edge and data available in a product-
ing and retail environment, and it grows specifications) than it is to achieve pub- and process-specific manner that best
at refrigerator temperatures. At present, lic health goals. Greater attention to meets FSOs.
a “limit-of-detection standard” exists preventing cross-contamination and The application of HACCP to pri-
for L. monocytogenes in an RTE food undercooking may have more impact mary production is particularly limited,
such that its mere detection is grounds on the public’s health than further re- because all the HACCP principles gen-
for legal action against the company ductions in the already small numbers erally cannot be achieved. Well-defined,
distributing the food and is the legal ba- of E. coli O157:H7 occasionally present science-based good agricultural practic-
sis for removing the food from the mar- in raw ground beef. es should be further developed for spe-
ketplace by regulatory agencies. A true Improving the scientific basis of cific commodities where appropriate.
farm-to-table food safety system would food safety programs will depend on Additional research will be necessary to
consider downstream handling and further understanding the pathogenicity better understand the microbial ecology
consumption patterns and epidemio- of microorganisms, including the infec- in these agricultural environments and
logic characteristics of cases; such a sys- tious dose of foodborne pathogens un- to formulate science-based recommen-
tem would not destroy foods that are der a variety of conditions, and a fur- dations for pathogen control.
unlikely to cause illness in the general ther reinforcement and implementation Routine microbiological testing is
population. In addition, some subtypes of proper hygienic and food handling useful for some purposes but not for
of L. monocytogenes found in or on practices of those responsible for pre- others. It can focus on pathogens of in-
foods have not been associated with ill- venting foodborne disease, including terest or on nonpathogenic microor-
ness, and additional research may dem- food producers and processors, public ganisms whose presence indicates con-
onstrate that some subtypes are not health professionals, retail food prepar- ditions favorable to the presence of
pathogenic. ers, and consumers. pathogens. Testing is useful for surveil-
Current technologies are also un- Regulatory agencies should work lance and HACCP verification purpos-
likely to consistently satisfy the demand with other public health officials and in- es. It also is used for validating and re-
for large volumes of fresh fruits and terested parties, including industry and validating processes.
vegetables that are free of harmful mi- consumers, to establish Food Safety Ob- However, microbiological testing of
croorganisms. Because these raw agri- jectives (FSOs). FSOs offer a means to finished product can be misleading, be-
cultural commodities are often con- convert public health goals into values cause negative results do not ensure
sumed without cooking, effective inter- or targets that can be used by regulatory safety. Testing has statistical limitations
ventions are needed that will diminish agencies and food manufacturers. FSOs, based on the amount of product sam-
or prevent the presence of pathogens. which can be applied throughout the pled, the percentage of product that is
Policies that result in minimizing con- food chain, specify the level of hazard contaminated, and the uniformity of the
tamination and preventing illness from that would be appropriate at the time a distribution of contamination through-

out the food. As the amount of contam- are due to viruses, and improvements borne illness. After GMPs and HACCP
ination in the food decreases, the food are needed in testing methods for viral provide adequately safe foods, the indi-
safety emphasis should focus on fur- pathogens in patients and in foods. viduals preparing the food must use
ther controlling processing conditions The range of pathogens associated proper knowledge, attitudes, skills and
through the application of science- with foodborne illness continues to in- practices to achieve food safety.
based HACCP plans. crease as new information identifies Consumers are sometimes inatten-
Because fresh produce undergoes pathogen/food associations. When new tive to their personal ability to reduce
very little processing, preventing con- food vectors are identified, risk man- the risk of foodborne illness. The public
tamination is the primary emphasis for agement decisions must consider the health community has the responsibility
ensuring the microbiological safety of best approach to control and preven- to discuss risk reduction strategies with
fresh fruits and vegetables. Thus, care- tion. Application of controls during consumers. Current risk communica-
ful consideration must be given to food production and processing may be tion is inadequate, and some consumer
growing conditions—including soil, necessary, although some hazards may perceptions and behaviors are not con-
water, manure, livestock, wildlife, pets, be better addressed at the consumer sistent with reasonable expectations re-
environmental pollution and effluent/ level through modification of exposure garding the safety of some foods. Com-
sewage, and humans—and their effect or susceptibility. munication with consumers to improve
on food safety throughout the food The person who serves as the host food choices and handling practices will
chain. for the foodborne pathogen is a major be an essential component of strategies
Many of the most prominent food- factor in the occurrence and character for the further reduction of foodborne
borne pathogens in the United States of foodborne disease. The individual’s illness. This approach has been success-
are carried by livestock and are princi- health, food consumption habits, and ful in the education of sensitive popula-
pally transmitted to food by fecal con- sanitation practices all directly affect tions, an activity that will necessarily
tamination. Manure, a significant vehi- the risk of foodborne illness. Hygiene, continue in the future.
cle for pathogens, is a growing source food preparation, and food handling Scientific data are a very substantial
of fertilizer. Use of manure fertilizer is and storage practices contribute to limiting factor in enhancing food safety.
an increasing environmental concern pathogen exposure. Food selection also Further research will continue to help
because it may contaminate water for contributes to the likelihood of expo- resolve complex problems and to pro-
drinking, irrigation, and recreation. sure. In addition, an individual’s under- vide information to improve the deliv-
Manure also is applied with or without lying health can have a significant im- ery of safe foods. Appropriate and ag-
composting to the soil used to grow pact on susceptibility to disease when gressive data collection throughout the
food crops. Manure used in the pro- exposed. food production and processing system
duction of food crops is of special con- An important contributor to micro- is essential for valid risk assessments
cern because the available scientific in- bial pathogenicity and human illness is and the resulting food safety improve-
formation is insufficient to ensure that the changing human population and its ments. Procedures must be implement-
foodborne pathogens are killed by cur- behavior. The elderly portion of the ed to obtain data from food manufac-
rent agricultural practices. Intensive U.S. population continues to grow, and turers in “penalty-free” environments so
farming practices can contribute to the large numbers of individuals have con- the data can be properly evaluated by
rapid spread of human and animal ditions necessitating the use of immun- public officials and the results made
pathogens by creating more concen- osuppressive drugs or drug combina- available to all interested parties.
trated environments for pathogens to tions with unknown effects, potentially It is difficult to conceive of a food
multiply and evolve and by generating increasing their susceptibility to food- safety system that responds effectively
larger quantities of subsequently con- borne illnesses. Many factors cause and efficiently to emerging microbio-
taminated food. changes in the immune system func- logical food safety concerns that does
An examination of the science re- tion, such as age, health conditions (e.g., not permit rapid changes in approach
veals that foodborne illness is caused AIDS, cancer), pregnancy, nutritional based on advances in science. Flexibility
by a complex combination of factors status, and antacid/medication use. to respond to new information and new
that must be managed on a continual Factors that suppress the immune sys- hazards will require unfettered data
basis. To achieve our public health tem increase the risk of foodborne ill- sharing. In addition, such a system can-
goals, everyone along the farm-to-table ness. not rely on the use of prescribed micro-
continuum must take responsibility for The increased understanding of in- bial control processes but instead must
their role in food safety management. testinal microflora and the immune emphasize validation and verification of
Foodborne disease is widely recog- system is providing opportunities for the methods used to assure food safety.
nized for acute effects on the gas- intervention strategies, such as probiot- The complex interrelationship of the
trointestinal tract but also includes ics, to facilitate human health and de- pathogen, host, and microbial ecology
other effects throughout the body. In crease susceptibility to foodborne ill- ensures a role for everyone in food safe-
addition, foodborne pathogens may nesses. ty management—industry, regulatory
cause chronic disease, which may occur The combination of proper hygiene agencies, public health officials, and
independently or accompany an acute and sanitation related to food handling consumers. A flexible, science-based
illness. Many of these chronic diseases and preparation, appropriate methods approach that relies on all parties to
have only recently been linked to food- of refrigeration and freezing, and thor- fulfill their role is our best weapon
borne pathogens. In addition, a grow- ough cooking of foods comprise a very against emerging microbiological food
ing proportion of foodborne illnesses effective approach to preventing food- safety issues.


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